Introduction

Primate communication has been the subject of a number of reviews and books. Marler (1965, 1968) has discussed the various principles and functions of communication in primates, and Altmann (1967) has described the theoretical structure of primate communication in terms parallel to those used in linguistics in his book on communication among primates. Altmann (1968) has also written an extensive review of social communication in all primates, which covers the literature up to 1966. More recently Ploog and Melnechuk (1969) havewritten a review that concentrated on visual and vocal communication in squirrel monkeys (Saimiri), including their work and that of their colleagues on brain stimulation. Jolly (1972) has compared communication systems in a number of New and Old World primate species. Peters and Ploog (1973) have written a general review of this area, which covers the literature up to 1972. See also the chapters in this volume on the Old World monkeys by Gautier and Gautier and on the apes by Marler.

The New World species have been looked at specifically in three papers. Moynihan (1967) covered specific behavior patterns in detail and introduced a number of hypotheses on the evolution and function of certain behavior patterns and displays. Data to test these hypotheses are only now beginning to appear in the literature. Snyder (1972) has reviewed briefly the literature for the marmosets and tamarins, and Epple (1975) has covered this area in much greater depth.

In this chapter I will primarily cover the literature from the mid-1960s to 1974 for the platyr-rhine species that have been studied in some detail. In Table 1 are listed the platyrrhine genera and species so the reader can easily determine which species still need attention. In Tables 2 through 5 the behaviorpatterns used by the New World primates are arranged according to their most prominent channel of communication: tactile (information conveyed while in physical contact), olfactory and visual (information conveyed up to intermediate distances), and acoustic (information conveyed even when out of visual contact). The species on which extensive information was available are included in the tables, and other species about which less is known are mentioned in the appropriate section in the text. The information presented has been gleaned from the literature, which varies tremendously in its amount of detail. For instance, a statement may be made that an individual of one species makes "threats," whereas another paper on a different species may go into great detail on each type of threat display, its channel, its orientation, and the circumstances that elicit it, and may even include information on threshold levels and associated behavior patterns. Thus in some places I may have unintentionally read more than what was intended and in other cases I have purposely eliminated a great deal of additional information, particularly in relation to associated behavior patterns. Nonetheless, the reader should be able to obtain a representative picture of our knowledge on communication in the platyrrhines as it exists in the present literature.

Our knowledge about communication in the primates, as in other animals, depends on our ability to observe and then later on our success in correctly transmitting this information. Others have pointed out (Lancaster, 1968; Marler, 1965; Ploog and Melnechuk, 1969) that language is a specialized ability limited to man, which allows information to be communicated about the environment, as I am doing in this chapter. It is separate and different from the vocal communication system possessed by all primate species, including man, which communicates emotion. Tool use has been suggested to be a possible reason for the development of language in man (Lancaster, 1968), but tool making and use occur in other species (Alcock, 1972; Eisenberg, 1973), for instance, chimpanzees (van Lawick-Goodall, 1968). I suspect that language evolved in man because division of labor prevented some individuals from obtaining personal knowledge of the environment, which they would need at some later time. My point in making this digression is to stress that nonhuman primates need and obtain the same information about their environments, but each individual gains this information first hand, in many cases with the help of other troop members or members of its family. Obtaining information about the environment by observational learning is entirely ignored here, even though the same communication channels are used by the receiver. However, the store of this knowledge and of knowledge about other individuals and neighboring troops permits a primate, or other animal, to make appropriate responses to the subtlest of cues or stimuli, ones that a human observer might be entirely unaware of. This is particularly important in captive studies, where normal behavior may be elicited, for a number of reasons, by inappropriate stimuli, and for that matter abnormal or inappropriate behavior patterns may be elicited by normal stimuli.

I have included in Table 1 a common name for each of the species discussed below for the reader's convenience; however, in the text I use primarily the scientific name of the species. The reason is that there are frequently several common names for each species and in some cases the common name may be applicable to more than one species. Readers who are interested in a particular species but are only acquainted with a common name other than that used here can consult Napier and Napier (1967:355-70).

Group Size and Social Structure

The size and social structure of monkey groups affect aspects of the communication system employed, and in turn the communication system helps to maintain the optimum group size and structure. The size of the group determines how many individuals need to be interacted with, and the social structure, including dominance hierarchies, determines how each individual to be communicated with should be addressed. The communication system helps to attract or repulse individuals, often of specific age or sex, to and from the group.

The marmosets and tamarins live in family groups including the adult pair and their young. Twins are usually born each year, and the male takes part in parental care. The adults dominate the young of their own sex, and attack and drive other adults away from the group (Epple, 1967, 1975). In captivity the dominant female may inhibit reproduction in subordinate females, even though these females have been copulated with. Though there is strong pair bonding between the adults, the male and female of neighboring pairs may copulate with one another. The pair bond is maintained by aggressive competition for the attention of the mate (Epple, 1975). Evidently, the young of successive years may stay with the parents so that family sizes of up to nine have been reported for Saguinus geoffroyi (Moynihan, 1970; Muckenhirn, 1967), six for S. midas (Thorington, 1968b), and eight for Leontopithecus rosalia (Coimbra-Filho and Mittermeier, 1973). These larger families may break up into smaller subgroups during the day (Muckenhirn, 1967; Thorington, 1968b), but several families may come together while feeding in large fruit trees (Coimbra-Filho and Mittermeier, 1973; Muckenhirn, 1967; Thorington, 1968b).

Callimico goeldii females, like the cebid females, give birth to one infant (Heltne et al., 1973), and thus may have slightly smaller family groups than do the other callitrichids.

Aotus trivirgatus, which also lives in a simple, parental family group, is the only New World species that is active at night, or more specifically just after sunset and before dawn, and sleeps in tree holes during the day (Moynihan, 1964; Perachio, 1971). Possibly because this species is most active in the dark or in poor light it has fewer visual signals than do other platyrrhine species. In captivity adults of the same sex "fight savagely" when placed together, and this aggressiveness probably helps to maintain the family unit by keeping it separate from other families (Moynihan, 1964).

Callicebus also lives in family groups, including the adult pair and one or two young. Neighboring families usually meet at specific sites along boundaries of their one-acre territories in the early morning and perform elaborate vocal and visual displays. Aggressive contact is rare. A female in estrus may briefly slip away from her mate to visit a neighboring male (Mason, 1966, 1968; Moynihan, 1966).

Squirrel monkeys (Saimiri) live in troops of up to three hundred individuals in undisturbed forests, but in the small patches of forest, which are common today, they live in troops of ten to thirty-five. The adult males live at the periphery of the troop, which consists of adult females and their young (Baldwin, 1968). During the mating season the males become "fatted" and sexually active, both physiologically and behaviorally (DuMond, 1968). The "fatted" males travel together and interact with one another agonistically. Their social structure is based on a linear dominance hierarchy, where dominance is most frequently expressed in penile displays. During the nonbreeding season the males travel together less often, but still give penile displays to one another. The adult males try to approach females by making rapid dashes into the troop, but they are chased off by the females and/or young, including infants (Baldwin, 1968). During the day pregnant females may form a subgroup separate from the main body of females with young (Thorington, 1968a). Play interactions may be rare or absent in some troops (Baldwin and Baldwin, 1973b). Allogrooming is rare (Moynihan, 1967), even between females in the main body of the troop (DuMond, 1968). Moynihan (1967) has suggested that allogrooming is rare in this species because penile displays, rather than grooming, are used in precopulatory behavior and because the individuals stay close to one another (see below); however, I suspect that cohesiveness in the main body of the troop is brought about by the pressures of the surrounding males, and that it is this pressure rather than a high level of gregariousness (Moynihan, 1967) that keeps the troop together.

Table 1

Scientific classification, common names, weight, and data on social structure.

In the capuchins (Cebus), troop size averages about twenty (Table 1), but varies depending on the stage in the population growth cycle (Oppenheimer, unpublished data). Adult males are part of the troop structure and receive grooming from all other members of the troop; females also groom each other and their young (Oppenheimer, 1969b). Adult females determine much of what the troop does and may even initiate troop splitting and formation (Oppenheimer, 1969a). The adult male or males interact with their counterparts of other troops during intertroop encounters. Agonistic behavior within a troop is rare, but may occur as an outgrowth of play or during the weaning period. Subgroup formation, which eventually leads to troop division, is probably a result of decreased affiliative interactions, rather than an increase in agonistic ones (Oppenheimer, 1968, 1969a, and unpublished data).

Howler monkeys (Alouatta) live in troops of ten to twenty individuals (Table 1), with twice as many adult females as adult males (Carpenter, 1965; Chivers, 1969; Neville, 1972a). They are the only New World primates that are solely vegetarian and are adapted to eating leaves. They rest much of the day, probably in order to digest the vegetable matter, and usually move only short distances (Richard, 1970). They have, particularly in the males, an enlarged saclike hyoid apparatus that acts as a resonating chamber (Schön, 1971), which allows production of vocalizations used to achieve intertroop spacing (Altmann, 1967; Chivers, 1969). In A. villosa the amount of time devoted to social interactions within the troop is low, primarily because so much time is spent resting (Richard, 1970). More social interactions, including allogrooming, occur in the red howler, A. seniculus (Neville, 1972b).

The spider monkeys (Ateles) live in troops of up to thirty-three individuals (Carpenter, 1935). The troops break up into subgroups of three, four, or more individuals during the day; the subgroups vary in composition from all male, to adult females and young, and/or a combination of both (Carpenter, 1935; Klein and Klein, 1971; Eisenberg and Kuehn, 1966). Eisenberg and Kuehn (1966) observed that the adult male of an A. geoffroyi group released on Barro Colorado Island spent only seven of twenty-six days with the adult females. This adult male, and some of the young males born after the release, spent many daylight hours traveling as a subgroup with a capuchin troop. Sometimes just before dusk he would give long calls that might bring the females to him (Oppenheimer, pers. obs.). The young of Ateles stay close to their mothers until two years of age and may continue to be nursed and carried by their mothers during this period. It may be that both the long association between mother and young and the tendency of males to attack females (Klein and Klein, 1971) influence the formation of separate subgroups.

Tactile Communication

The importance of tactile communication in primates, as well as in other animals, has been indicated by the intensive research of the Harlows and their colleagues on rhesus monkeys (Harlow, Harlow, and Suomi, 1971). The opportunity to receive positive feedback through tactile communication with the mother allows the young to develop normal patterns of social behavior and the requisite physiological responses that underlie them. The behavioral units of tactile communication are usually characterized in terms of their visual components, rather than in relation to the message conveyed. This is probably because a number of tactile behavioral units may occur under similar circumstances, and the difference in message content between them, if any, is not immediately obvious to the observer.See, for instance, the paper by Maurus and Pruscha (1973), where cluster analysis is used to determine which behavioral units are similar.

The smaller species—the marmosets, tamarins, and the night monkey (Aotus)—probably all sleep in tree holes or crotches of trees at night (Table 2). In such small spaces, probably all members of the family sleep in contact with one another. Moynihan (1967) has suggested that this passive contact may fulfill, at least in part, the social function of allogrooming (see below). He suggested this because his initial observations of Aotus and Saguinus geoffroyi indicated that they did very little allogrooming; however, more recently (Moynihan, 1970) he has observed that individuals of Saguinus geoffroyi do engage in social allogrooming. Thus the social function of passive contact while sleeping is now questionable and would be best studied under laboratory conditions. Probably all species, large or small, seek contact with specific members of their family or troop while resting or sleeping. Such contact, which is actively allowed, probably does play a role in developing cohesiveness in the group.

Huddling is related and may be of shorter duration than the above behavior, but the relative positions of the individuals and the extent or type of contact have not been adequately described in the literature (Table 2).

Hugging or embracing is a much more specific type of contact, which has different forms and functions among the different species. Probably in all species it is unilaterally performed by a mother to her infant; it has been described for Alouatta villosa as cuddling (Baldwin and Baldwin, 1973a). Mutual cuddling, or hugging, has been observed in three species (Table 2). It serves as a greeting or contact-promoting behavior that tends, at least in Ateles, to reduce agonistic tendencies (Klein and Klein, 1971). It is an adult behavior pattern in Callimico (Lorenz, 1972) and Ateles (Eisenberg and Kuehn, 1966) and an infant behavior pattern in Cebus capucinus (Oppenheimer, 1968, 1973). In Ateles, and possibly in Cebus, one of the individuals sniffs the sternal gland of the other. Thus this behavior pattern has both tactile and olfactory components and will be discussed further in the next section.

Carrying is primarily a parental behavior pattern. In the monogamous species—the marmosets, tamarins, and the owl and titi monkeys (Table 1)—the male parent does most of the carrying (Eisenberg and Kuehn, 1966; Epple, 1975; Heltne et al., 1973; Snyder, 1972), but juveniles may also eagerly carry young (Kleiman, pers. comm.). Although this behavior on the part of the male may have been selected for because marmosets and tamarins usually give birth to twins (Epple, 1975), the behavior also occurs in Aotus, Callicebus, and Callimico, where the female usually gives birth to only one infant at a time. It is more likely that the monogamous social structure of these species has selected for behavior patterns that strengthen the cohesiveness of the family unit, i.e., paternal carrying. Capuchin (Cebus) infants are often carried by juveniles during play, and on rare occasions adult male capuchins and adult male spider monkeys will carry an infant for short periods (Oppenheimer, pers. obs.; Eisenberg, 1976). After a howler monkey (Alouatta) female has been shot, an adult male will retrieve and carry the infant (Carpenter, 1934). While two individuals are in such intimate contact, other signals may well occur. Captive capuchin infants have been reported to squeeze or knead the skin of their carriers when they were disturbed (Oppenheimer, 1973). This has also been observed in free-living C. capucinus (Curt Freese, pers. comm.).

Table 2

Tactile communication

While riding on the back of another individual, an infant usually curls its tail around the base of the carrier's tail, as in Cebus (Oppenheimer, 1968), or the body, as in Saimiri (Baldwin, 1969), in order to secure its position. When giving assistance during an agonistic encounter in Ateles, the assister will wrap its tail around the assistee's body or tail (Klein and Klein, 1971). In Saguinus geoffroyi, one adult may loop its tail over its partner's body while they are sitting together; this additional type of contact may help to strengthen the pair bond (Moynihan, 1970). Ritualized tail twining occurs between paired adults in Aotus and Callicebus (Moynihan, 1966) and would seem to function as a positive tactile communication.

In monogamous species, allogrooming is interpreted as being, in part, sexually motivated, because it occurs primarily between the two adults, who are of opposite sex, and may be associated with sexual activities between these two individuals (Table 2). In Aotus allogrooming specifically occurs just prior to and after copulatory interactions, when the mates are sitting side by side in contact; however, in addition to its proposed function to stimulate sexual motivation, it still plays its general role of reducing hostility between the mates (Moynihan, 1964). In those species where there are two or more adult females in the social unit, allogrooming tends to be primarily a contact-promoting behavior, which helps to set up and maintain the social structure of the troop. Adult males may receive a lot of grooming attention from the other troop members, but most grooming is done by the adult females and is directed to specific other adults, or to young, particularly newborn infants (Oppenheimer, 1969b). Allogrooming in Ateles appears to be a means of maintaining a relationship once it has been established (Eisenberg and Kuehn, 1966).

In addition to the species mentioned in Table 2, allogrooming has been observed in both species of Pithecia and in Cacajao rubicundus; but it has not been observed in Cebuella pygmaea, where captive conditions may well inhibit such activity (Moynihan, 1967). Allogrooming tends to be rare in Saimiri, where it is primarily a maternal activity, and in Alouatta, both of which genera have evolved specialized precopulatory displays (Moynihan, 1967). It is interesting to note that social allogrooming is more frequent in A. seniculus, which has a less highly evolved precopulatory tongue display, than does A. villosa (Neville, 1972b). It may also be that in Alouatta the vocal interactions between troops act as an outside force that contribute to intratroop cohesiveness, and this in turn lessens the need for social allogrooming. Put another way, selection in Alouatta may have led to a "social" strategy, where energy is expended in repulsing individuals outside the troop, rather than expended by attracting individuals within the troop, but both strategies would result in intratroop cohesiveness. My personal observations of A. seniculus in Venezuela suggest that its intratroop vocal interactions are less frequent than those of A. villosa on Barro Colorado Island in Panama, a condition that could explain the different frequencies of social allogrooming in the two species. More detailed discussions of allogrooming can be found in Moynihan (1967) and Sparks (1967).

Touching another individual with the hand seems to reassure one or both individuals (Table 2). In Callicebus and Cebus it is used to reassure the partner while both threaten a third party. In Cebus the hand touch usually includes draping the arm around the partner's shoulders and may shift into chest-to-back contact (Fig. 1; Oppenheimer, 1968, 1973). Touching with the hand may also occur during play, or when an immature C. albifrons approaches an adult male and touches the male's face (Bernstein, 1965). In Saimiri sciureus touching may occur during play, but a heavier hand touch or possibly a grasp, described as "putting hand on," occurs when a male threatens another with a genital display (Baldwin, 1968). In this case, the hand is probably used to support the displayer as well as to hold the second party in an appropriate position (see genital present below).

Placing the face against another and moving it back and forth, nuzzling, has been reported for three species (Table 2), but probably is more widespread. It tends to be either a maternal or an adult sexual act.

Fig. 1. Cebus capucinus assistance position showing adult female with chest in contact with adult male's back. Usually the dominant, i.e., the male, is on top. Female making medium-intensity (only lower worn canines exposed) open-mouth-bared-teeth face threat toward observer. Male in display posture, frowning and staring at observer. Male's face square and forehead almost naked with some very short white hairs. Female's face vertically oval with long white and dark hairs on forehead. Photo taken of members of troop A\ (Oppenheimer, 1968, 1969) on Barro Colorado Island, Panama Canal Zone.

Licking, touching, and manipulating the genitalia of the opposite sex (Table 2) usually follow sniffing, which will be discussed later (Table 3). Whereas sniffing has been reported for most New World species, contact between the tongue or hand and the genitalia has only been reported for the Cebidae and for Callimico, which is an intermediate form that is sometimes placed in this family (see Napier and Napier, 1967:371). If this difference does exist, it may indicate an underlying hormonal-pheromonal and/or neurological difference between the two New World families. In some species only one sex, either the male or the female, performs the behavior, whereas in other species both sexes are reported to do it. It is characterized as a sexual or contact-promoting behavior and probably causes an increase in sexual motivation when the female is in estrus.

Female mounting and thrusting tends to be primarily a play or homosexual activity (Table 2); however, a Cebus capucinus female has been observed in nature to alternate her mounting and thrusting with that of a male (Oppenheimer, 1968, 1973).

Adult male mounting and thrusting obviously occurs in all species, even though observations are lacking for some. Among juveniles it occurs during play, but among adults it is sexually motivated. Bouts of thrusting between males and estrous females may last from twenty seconds to ten minutes (Table 2). Subadult male capuchins (C. capucinus) have been observed to mount and thrust upon each other, and on adult female Ateles geoffroyi in the wild on Barro Colorado Island (Oppenheimer, unpublished data; Richard, 1970). The use of visual sexual displays in dominance interactions does occur in some species (see below, Table 4), and thus may preclude the use of a tactile sexual behavior for this purpose. Possibly one could view the combined "put hand on" and genital display of a male Saimiri threatening another (Baldwin, 1968) as a ritualized, redirected, intention movement to mount, but it seems more likely that this combined display has evolved for the purpose of transmitting an olfactory signal.

Wrestling, which includes grappling, pushing, pulling, and mouthing, occurs primarily during play, but also during agonistic encounters, where mouthing turns to biting. The information obtained during play from performing these behavioral acts allows an individual to learn the extent of his or her abilities, whereas the information received from immediate feedback, in terms of the partner's response, places general, as well as specific, limits to the expression of these acts and helps to establish the social structure of the group (Carpenter, 1934). See Loizos (1967) for a detailed discussion of play behavior, and Baldwin and Baldwin (1973b) for a discussion of the role of play in squirrel monkeys. In many species these play activities are most obvious in the young, particularly the males, but they disappear as the play gets more intense (Baldwin, 1969; Carpenter, 1934). Vocal and visual displays then become the main channels of low- to medium-intensity communication, at least among the males, whereas tactile communication in the form of allogrooming may become more prominent among the females. Agonistic wrestling has been observed in a number of the species, particularly in adults (Table 2); however, in adult spider monkeys (Ateles) these behavior patterns retain their play aspects during greeting interactions (Klein, 1971). Pushing and pulling in some species have become semiritualized forms of threat (Table 2).

Tagging, a repeated behavior that is intermediate between touching and hitting, is reported to occur in howlers (Alouatta) during play (Bernstein, 1964) and during agonistic encounters (Neville, 1972b). It has been observed in C. capucinus, particularly when a juvenile is harassing an adult female (Oppenheimer, 1973).

Hitting is a frequently observed agonistic behavior pattern among the species (Table 2), but it has also been reported to occur during play in Alouatta seniculus (Neville, 1972b). Kicking, another agonistic act, has only been reported in two species, and hip thrusting in one (Table 2).

Chest-to-back contact, in contexts other than mounting and carrying, has only been reported for four species of cebids. It was observed incidentally in Ateles when a captive adult female solicited mounting from a male by sitting in his lap (Eisenberg and Kuehn, 1966). It functions as an extreme threat to the individual on the bottom in Saimiri sciureus when it follows "put hand on" during a genital display and hip thrusting (Baldwin, 1968). In Cebus (Fig. 1) it occurs as an assistance behavior when one individual reinforces the threat of another toward a third party (Bernstein, 1965; Oppenheimer, 1973; Oppenheimer and Oppenheimer, 1973). In other species assistance behavior may only involve touching with the hand or tail (Table 2). In Saimiri sciureus contact involves threat so that assistance takes the form of merely standing side by side while performing threatening genital displays toward the third party (Baldwin, 1968). Noncontact assistance is the mildest form of assistance in other species, such as C. capucinus (Oppenheimer, unpublished data) and C. nigrivittatus (Oppenheimer and Oppenheimer, 1973).

Although biting, the ultimate agonistic act, has been reported for most species, mouthing, warning, and sham bites have only been reported for the Cebidae (Table 2). Most of the mouthing occurs during play, whereas the warning or sham bites tend to be mild agonistic forms.

Olfactory Communication

Two recent reviews of scent marking in mammals (Eisenberg and Kleiman, 1972; Ralls, 1971) covered a number of points that are relevant here. Feces, urine, and secretions from specialized skin glands do play a role in social communication. The resulting odors or pheromones are used to mark an area, to facilitateindividual or group recognition, to indicate the sexual status of females, and to inhibit the sexual development of other members of the group; a single odor can have one or more functions. Releasing of the scent, or scent-marking behavior, can be brought about by the approach of a subordinate individual or one that is not accepted, such as a stranger; and the scent can function to increase the confidence of the scenter by surrounding the scenter with an odor familiar to it, as well as to threaten or make less confident nearby individuals by disrupting the odor field around them (Eisenberg and Kleiman, 1972). More specifically, for the platyrrhines the olfactory system can be used to communicate information such as the "sex, age, social rank, territory, and more detailed biological facts" (Epple and Lorenz, 1967).

In some cases special movements have been evolved for distributing the scent (Ralls, 1971), and it is these visual components of the behavior or the movements of the recipient of the odor that are most obvious to the human observer and which are primarily indicated in Table 3. The absence of visual components of marking behavior is not proof that olfactory communication is lacking in the species. In my review of the literature only two species appear to lack the specialized behavioral components (Table 3), Pithecia monachus and Cacajao ruhicundus (Moynihan, 1967), but the behavior of neither species has been studied intensively.

Sternal glands and/or the related gular and epigastric glandular areas have been found in almost all the New World species, including P. monachus and C. ruhicundus (Epple and Lorenz, 1967), and use of these glands has been documented in some. Epple and Lorenz (1967) have indicated the morphological differences between the species and have found that the glandular area of the Callitrichidae (excluding Leontopithecus) and Aotus is situated "at the articulation of the sternum and claviculae," a brush of hairs just caudad to it, and caudad of the brush "a ribbonlike field of nearly naked glandular skin. . . ." The sternal glands seem to reach their fullest development in the dominant males. For other details see Epple and Lorenz (1967). Some species also have suprapubic and circumgenital scent glands (Epple, 1971, 1972a). Epple (1972a) has reviewed the olfactory behavior in marmosets and tamarins and her paper should be consulted.

Although most of the information to be presented below will deal with the visual components of marking behavior, two studies of the ability of platyrrhines to discriminate between odors need to be mentioned. Epple (1971) presented adult Saguinus fuscicollis of both sexes with wooden perches that had been marked with urine and glandular secretions of a separate set of adults. The nine test animals spent the same amount of time sniffing the male and female marked perches, but marked with their own urine and glandular secretions those perches having the odor of strange males more frequently than the perches having the odor of strange females. Thus they were able to discriminate between the odors of the two sexes. In addition, the most aggressive animals showed the most interest in the perches, whereas the less aggressive tended to avoid marked perches. Another study with infant Saimiri sciureus four to twelve weeks of age showed that they preferred surrogate mothers having their own odor on them to clean surrogate mothers, and were able to distinguish their own odor from that of another. Thus odors can be important to squirrel monkey infants and may help them to distinguish their mothers from other individuals (Kaplan and Russell, 1974).

Table 3

Visual components of olfactory communication

Release of feces and urine are basically autonomic responses elicited by fear (Eisenberg and Kleiman, 1972). They have been reported to occur in four species of cebids. In addition to urinating and defecating when frightened, Aotus has been observed to vomit (in captivity) under the same conditions, but none of these behaviors were considered a signal (Moynihan, 1964). Release of urine and feces in the other three species is triggered by strong excitement or alarm (Table 3). It certainly could be debated whether urinating and defecating are ritualized in these circumstances, but just as certainly their odorif-erousness makes it reasonable to assume that their occurrence is noticed by nearby individuals and that their predictability would allow a distress or presence-of-disturbance signal to be conveyed.

Ritualized urine washing or rubbing, where the urine is applied to the palms and rubbed on the soles, and in Cebus capucinus (Oppenheimer, 1973) to the tip of the tail, is also reported to occur only in the Cebidae (Table 3). In Saimiri sciureus adult males and females urine rub after doing genital displays during a sexual sequence (Latta et al., 1967; see also Castell and Maurus, 1967). In Cebus capucinus and C. nigrivittatus it is most frequently the adult males that urine rub, usually when they have been disturbed by a conspecific or a human observer, and it seems to have both self-reassuring and identifier functions (Oppenheimer, 1968, 1973; Oppenheimer and Oppenheimer, 1973).

A somewhat similar behavior of rubbing substances into the fur has also been noted for free and captive individuals of C. capucinus (Oppenheimer, 1968) and captive C. apella (Nolte, 1958). In captivity a wide range of strong-smelling substances, like vinegar, onions, and tobacco or tobacco smoke, can elicit rubbing and are rubbed into the fur. In the free-ranging C. capucinus such behavior was rare, but on two occasions strong-smelling plants were vigorously rubbed into the fur on all parts of the body. In one situation several individuals did it together, and in the other it was performed by a female that was alone (except for the observer) at the time (Oppenheimer, 1968). In terms of the Kleiman hypothesis (Eisenberg and Kleiman, 1972:26) these individuals rubbed to reestablish their optimum odor field, or possibly to create a supraoptimum one, which gave them a sense of security.

Estrous females of two species, Saguinus geoffroyi (Epple, 1967) and Callimico goeldii (Lorenz, 1972), urinate on their tails, which they curl up between their legs. Moynihan (1970) did not observe the urine wetting, but did observe tail coiling prior to and in between mounting and thrusting by a male (see visual displays below). This display could be used to help disperse pheromones that indicate that the female is in estrus and receptive. The urine of estrous females is reported to be a sex attractant in a number of species and probably is for all (Table 3).

Genital displays, including release of urine or a glandular secretion, are reported for members of both New World families. The marmosets Cebuella pygmaea, Callithrix jacchus, C. argent at a, and C. geoffroyi all lift their tails and expose the analgenital area when threatening a subordinate who approaches and sniffs; adults of both sexes perform this display (Epple, 1972a). Adult male Saimiri present their genitalia frontally by lifting one leg away, and release a small amount of urine. This may occur as a threat or after licking a female or after a female has urinated or urine rubbed (Baldwin and Baldwin, 1972). When used as a threat the dominant male will approach, display, and place his hand on the subordinate's head, which apparently forces the subordinate to sniff the dominant's genitalia (Baldwin, 1968).

Rubbing of the anal-genital area on the substrate is primarily a behavior pattern of the marmosets and tamarins, though it has been observed in the cebids aswell (Table 3). Such rubbing is usually done while in a sitting position, which would place the circumgenitaland circumanal glands in contact with the substrate or a conspecific (Epple, 1972a). This type of behavior iselicited in sexual, dominance, threatening, and frustrating circumstances. It is rare in Saimiri (Moynihan, 1967) and is thought to be a type of autogrooming or cleaning behavior in Alouatta seniculus (Neville, 1972b) and Callicebus moloch, though on one occasion an adult Callicebus rubbed while carrying an infant (Moynihan, 1967).

Pull rubbing (Moynihan, 1970) or rubbing the suprapubic glands on a substrate occurs in Saguinus and Leontopithecus and appears to help strengthen the pair bond or to assert dominance. It may occur along with anal-genital rub and with chest rubbing (Epple, 1972a).

Chest rubbing or rubbing of the sternal and/ or epigastric gland(s) occurs in many of the platyrrhines (Table 3). It is usually done by the dominant male and is interpreted to be a threat in some species and an assertion of the individual's identity in others (see the Kleiman hypothesis above). The marmosets and tamarins seem to rub the gland directly on the substrate; the cebids may do this, but they usually rub the gland with a hand or foot. Callicebus may squeeze the gland with a hand, as well as rub it (Moynihan, 1966), and Saimiri may touch it with a foot (Baldwin, 1968). In addition, three cebid species mix the sternal gland secretions with either urine or saliva. The fatted males (in sexual condition) of Saimiri sciureus urine rub and then lift the wet foot to the sternal gland. This behavior usually occurred when a male was about to approach a group of females who were likely to chase him away (Baldwin, 1968). Lagothrix (Epple and Lorenz, 1967) and Ateles (Klein and Klein, 1971) both rub their chests with their hands and then may raise the hand to the mouth for saliva, after which they continue to rub the chest. In some cases Ateles drools saliva onto the chest or onto the object being rubbed on. This behavior was also elicited in Ateles by mildly or strongly stressful situations or exposure to celery or green onions (Klein and Klein, 1971), which suggests a similarity to urine rubbing and rubbing of plants into the fur, as occurs in other species, such as Cebus capucinus (see above).

There are conflicting reports as to whether certain species chest rub. Epple (1972a) has observed it in Saguinus geoffroyi but Moynihan (1970) has not. Epple and Lorenz (1967) have observed it in three captive Cebus capucinus, but I have never observed it in the wild; the only indication of functioning sternal glands that I observed was when an infant dropped its head to the chest of another infant during a hug, and even this behavior was rare. Similar sniffing occurs frequently in Ateles during embraces (Eisenberg and Kuehn, 1966). Moynihan (1967) had not observed chest rubbing in Ateles geoffroyi, but others have (Eisenberg and Kuehn, 1966; Klein and Klein, 1971; pers. obs.).

Alouatta seniculus, which has a gular scent gland (Epple and Lorenz, 1967), has been observed to rub this gland on the substrate prior to approaching a conspecific (Neville, 1972b). Cebus apella, which lacks a gular gland, has been observed to urinate on an object and then to rub its neck on the object (Dobroruka, 1972).

All these glands, as well as urine and urinemarked spots, are sniffed by conspecifics. In some cases after sniffing the conspecific may mark (Epple, 1971). Sniffs are also directed at the body in general, at the armpit and at the face (Table 3). Moynihan (1964) notes that Aotus has large apocrine and sebaceous glands on either side of the nose. Since adult Aotus sniff each other's faces just prior to copulating, it seems likely that these glands also function in olfactory communication.

The genitalia of the platyrrhine species are quite varied in external morphology. One of themost striking, and initially deceiving, forms is the long pendulous clitoris of the Ateles female. Klein and Klein (1971) have suggested that this elongated clitoris, which tends to retain a small amount of urine, has been evolved to mark the environment wherever it touches, and that this in turn makes it easier for the male to locate the female. Also, when males make contact with the clitoris with their hands they are more likely to obtain a urine sample on their fingers, which they can then smell and lick.

In addition to the information conveyed over the short term by olfactory communication, there are hints of long-term effects or responses. Baldwin (1968) suggests that hormonal activity in submissive male squirrel monkeys (Saimiri) might be inhibited by pheromones released in the dominant male's urine during a penile display, which the submissive male is forced to inhale. The presence of a dominant male Callimico goeldii retards sexual development in other males (Lorenz, 1972). Similarly the presence of a dominant female marmoset may prevent other females from producing young, even though copulation takes place. Once removed from the presence of the dominant female, these females may produce young (Epple, 1975). See Eisenberg and Kleiman (1972) for the pertinent details on olfactory inhibition of reproduction in rodents.

In summary, it appears that most platyrrhines have at least two, and some have as many as four, types of olfactory display. These displays have sexual, alarm, threat, and self-identification functions. They may also have physiological effects on the hormonal systems of other group members. It is hoped that the isolation of specific substances and the elucidation of their activity will occur soon. But even if it does we still need more observations and quantitative analyses of olfactory communication.

Visual Communication

Visual communication can be divided into three categories: (1) postures, and movements of part or all of the body; (2) piloerection displays; and (3) facial expressions (Moynihan, 1967). In some situations all three types can occur as part of a complex display, such as when directing a threat display toward a predator or a human. Moynihan (1967, 1970) has reviewed the occurrence of gestural and piloerection displays in a number of New World species, and Andrew (1963) and van Hooff (1967) studied the facial expressions of some platyrrhines in their studies of communication in primates.

GESTURES

All species have "look at" and most likely "look away" behavior patterns, though it is unritualized in its general form. Prolonged looking at or staring is usually interpreted as a threat, but it should be regarded as an expression of interest that may have a number of different motivations, including aggression. These motivations are expressed by additional facial expressions, body gestures, or acoustic signals. Looking away can indicate alarm or a desire to avoid contact. Aotus and Callicebus have a specialized form, which involves lowering the head (Moynihan, 1964, 1966). Repeated looking at or glancing and looking away (at another monkey or a human) in Cebus capucinus usually induces approach and assistance by a third, usually more dominant, individual during an agonistic interaction (Oppenheimer, 1973); a dominant male will look away when stared at by a human observer (Oppenheimer, pers. obs.).

Submissive crouches or huddles occur during dominance interactions in Saimiri and prior to copulation in Alouatta villosa females (Table 4).

Freezing is a related behavior, which occurs when an individual is alarmed, or in the case of Callimico goeldii females, it occurs just prior to copulation. It is not clear from the descriptions in the literature whether freezing also includes a lowering of the body. This may vary from species to speciesor with the type of motivation. Crouching or freezing as an alarm or submissive response occurs in species of both New World families.

"Lie on back" may be another common behavior pattern, but it has only been noted in the literature for three species. It is an appeasement gesture that inhibits attack, or in juvenile Cebus capucinus during play it encourages contact (Oppenheimer, pers. obs.). This behavior has apparently been ritualized in squirrel monkeys and has the added component of side-to-side rolling. This back rolling occurs during play and is performed by the dominant animal in order to induce others to approach and make contact (Castell, 1969). Back rolling is also performed by female howler monkeys after copulation (Carpenter, 1934), but the subsequent behavior has not been noted; and it was performed by a captive female Saguinus geoffroyi after a male failed to respond to her invitations to copulate (Moynihan, 1970:43).

Soliciting allogrooming consists of an individual's positioning itself in front of another and sitting face to face with eyes averted or lying prone and presenting the back. Saguinus geoffroyi solicits by erecting the hair on the nape (Moynihan, 1970).

Soliciting for play probably takes many forms. During sexual play female Saimiri sciureus entice the male partner by assuming odd postures, such as looking between the legs or hanging by the feet. The females may allow the male to make contact, but then dart away (Latta et al., 1967). Play among juveniles and subadult whitefaced capuchins (Cebus) is solicited by similar patterns, as well as by lying on the back (Oppenheimer, pers. obs.).

Soliciting sexual mounting by the female takes a wide variety of forms in the different species (Table 4), including crouching with the tail aside, backing into the male, mounting the male (C. capucinus), curling the tail up between the legs, and presenting the tongue (see below). More than one of these patterns may occur in a single species: a female Alouatta villosa may tongue flick, present her rump, urinate, and take a submissive crouch posture (Carpenter, 1934). Tongue protrusion or flicking is a common sexual behavior that is performed by both sexes (see below).

Head shaking can occur from side to side, back and forth, or up and down and may include shaking of the body, depending on the species (Table 4). In most cases the individual giving the display is approaching a dominant individual, either a conspecific or a human. Saguinus geoffroyi may in addition head shake at a predator (this may actually be swaying, see below) or at its female mate during copulation (Moynihan, 1970). This behavior can be described as appeasement during an ambivalent approach, one which may include components of escape. In Cebus capucinus the head shake is accompanied by grinning, frowning, and a vocalization called guttural chatter (Oppenheimer, 1973). Andrew (1963) describes such a display complex, plus tongue protrusion and eye closure, as being or having evolved from a protective response to a noxious odor or taste, and states that these responses can be elicited when an individual approaches another who may attack. In C. capucinus the dominant individual ignores the head shaker and thus allows the approach to continue (Oppenheimer, 1968).

Tail-rump shake involves side-to-side movement of the tail. It is done by Aotus and Saguinus geoffroyi only during sit rubbing, though sit rubbing can occur without tail movement. In S. geoffroyi sit rubbing occurs when an individual is frustrated or engaged in a sexual or dominance interaction; in Aotus it occurs under similar circumstances (Moynihan, 1964:52, 1970:20). In the other species tail-rump shaking occurs without anal-genital rubbing and is associated with strong excitement, tantrums, and sexual and agonistic behavior. It is also a signal or part of a movement by a mother to get an infant off her back (Table 4).

Table 4

Visual Communicatione

Bringing the tail forward under the body is associated with alarm in Callithrix jacchus (LeRoux, 1967) and Saguinus geoffroyi (Moynihan, 1970). With the tail in this position, the tip may be coiled (tail tip coiling), a response that indicates a higher level of alarm and may function as "a warning and/or appeasement . . . display" in captive S. geoffroyi housed in crowded conditions (Moynihan, 1970).

Upward tail coiling, where the complete tail, rather than just the tip, is coiled and is held between the legs, is performed most frequently by sexually motivated S. geoffroyi females and less frequently by sexually thwarted males in captivity. At least in females the behavior is thought to indicate sexual receptivity (Moynihan, 1970). Upward tail coiling plus wetting the tail with urine has been observed in captive female S. geoffroyi (Epple, 1967) and Callimico goeldii (Lorenz, 1972) during sexual interactions. Moynihan (1970:48-52) discusses this behavior pattern in some detail and gives suggestions as to how it might have evolved into a sexual soliciting act. I have also observed this behavior, without urine wetting, in captive S. geoffroyi and thought it indicated alarm on the part of both male and female performers during sexual encounters. Since the lower-level tail tip coiling is done in response to alarm, and urine release may also be stimulated by alarm or invasion of one's individual distance, further studies would be of interest.

There are two major types of genital displays. In the family Callitrichidae species that display their genitals (scrotal sac and labia) do so by lifting their tails and orienting their rump toward the intended receiver, while keeping hands and feet in contact with the ground (see Epple, 1967: Figs. 8 and 9). After the tail is raised pheromones may be released (Epple, 1972a). This display is done by both sexes and is thought to be an aggressive threat (Epple, 1967, and 1975). In the family Cebidae the genital present is done frontally, with the chest raised, legs spread, and penis or clitoris erect (Castell, 1969; Eisenberg and Kuehn, 1966; Winter, 1968). In Saimiri the genital display is done at a distance, from 10 cm to 4 m, and the displayer is erect; it is also done in contact, with the displayer bending over his partner and seeming to thrust his penis in the partner's face (Castell, 1969) while pressing the partner's head down (Winter, 1968). The distant or open position is used by young and by adult females and appears to indicate frustration or self-defense. The contact or closed position is used by males during dominance and courtship interactions (Ploog, 1967). A captive Ateles male was observed to perform pelvic thrusts with an erect penis in front of a femalebefore copulation (Eisenberg and Kuehn, 1966); however, in the wild such behavior was not associated with sexual behavior, but rather with resting in a group or alone, while being groomed, while playing, or after homosexual hugging (Klein, 1971). In Alouatta seniculus both the male and female may have erections during a sexual interaction (Neville, 1972b).

The display posture has been observed during an agonistic interaction (Table 4) in most species, and involves orienting toward and looking at another individual with the back slightly arched. While in the display posture other aggressive displays may be performed, such as bouncing or the open-mouth-bared-teeth face. Though the display posture is usually done while on all fours, Aotus and Callicebus may sometimes stand up to transmit their threat (Moynihan, 1964, 1966, 1967). S. geoffroyi always stands up during display posture so that its intimidating white venter is fully exposed toward the second party (Moynihan, 1970).

Although related because of the arched back, stiff walking usually occurred at different times, at least in Cebus capucinus; it occurred most often when free-living subadult or adult males came to the caged capuchins and strutted across the tops of their cages or along a limb in a nearby tree. The display seemed to indicate unchalleneged dominance (Oppenheimer, 1973). Such a display has been observed in captive marmosets, where it indicates dominance, and in Callithrix jacchus it may also be performed during sex play (Epple, 1967). A possibly related display, pacing, is done by Saimiri sciureus males in front of a receptive female prior to copulation (Baldwin, 1968); however, no mention is made as to whether the male's back is arched, and the stationary display posture is apparently lacking from the Saimiri behavioral repertoire (Table 4).

Bouncing and intention movements to lunge are performed by Cebus capucinus while in the display posture (Oppenheimer, 1973), and swaying is performed by marmosets while sitting (Moynihan, 1970). In all cases these movements are done toward a human or a predator and may function as a defensive threat or alarm. Swaying is a side-to-side motion, though in Callicebus there may also be a vertical component (Moynihan, 1966). Young capuchins (Cebus) may make short forward and backward movements as if they were going to lunge, whereas in adults the movement, bouncing, is in the vertical plane (Oppenheimer, 1974). Such behavior, which may be accompanied by vocalizations, attracts the attention of the predator to the performer and may also alert other troop members to the presence and location of danger and allow them time to escape. Moynihan (1966) suggests that swaying may inform the predator that it has been seen and thus for the moment terminate the hunt.

Lunging at is an agonistic behavior pattern reported for a number of species and may function as a threat (Table 4). Lunging at can be considered a preliminary movement to grappling or chasing.

Chasing is a play activity, at least in the young of some species, but in adults it is primarily aggressive (Table 4). Running away is assumed to occur in all species, particularly those where chasing is reported.

Banging of objects, as a signal, has only been reported for three species of cebids (Table 4). It appears to be a male aggressive behavior. Freeliving Cebus capucinus males on Barro Colorado Island did this when they visited the cages where capuchins were kept captive; they lifted and dropped sheet metal on the cage roof and jumped up and down on it. This behavior, in part, would seem to have the same motivation as branch shaking, which occurs in the trees (Oppenheimer, unpublished data).

Branch shaking has only been reported for cebids, and it functions as a threat display (Table 4). Saimiri sciureus males branch shake at sexually nonreceptive females (Baldwin, 1968). In Cebus capucinus branch shaking is generally stimulated by the presence of a human observer, but less frequently it may also be used as a general threat within the troop; branch breaking, without branch shaking, was primarily observed to occur at the start of intertroop encounters (Oppenheimer, 1973). Moynihan (1964) has suggested that branch shaking and breaking may not occur in Aotus because they are too small; however, they have approximately the same weight as Saimiri (Table 1). This display appears to be absent in all species that live in monogamous pairs. It may be that in such species the family members tend to disperse less and thus displays that attract a predator's attention might endanger the whole group.

PILOERECTION

Piloerection is a common display that accompanies other types of threat behavior or may be triggered by alarm (Table 4). Moynihan (1967, 1970) discusses this behavior in detail. Piloerection on the tail is a specialized alarm display that has been observed in Callithrix jacchus and Saguinus geoffroyi (Moynihan, 1970).

FACIAL EXPRESSIONS

All species do have a "relaxed face" (van HoofF, 1967), but there is usually little mention of it in the literature.

Grinning in the Callitrichidae in combination with flattening of the ears appears to be a defensive threat (Epple, 1967), and in the Cebidae it is an appeasement or submissive display that may be used by the dominant or the subordinate animal (Table 4). In Cebus capucinus, infants may combine the grin with a frown and a lateral head shake when approaching a dominant animal, usually the troop's adult male (Oppenheimer, 1968, 1973). In C. apella the grin is accompanied by raising of the eyebrows (Weigel, 1974). The grin involves pulling back the corners of the mouth while keeping the jaws shut. There may be some confusion with low-intensity open mouth-bared-teeth face. Moynihan (1966) has described a "baring the teeth" face in Callicebus, which is similar to the Cebus grin, except that the corners of the mouth are not retracted.

Fig. 2. Cebus capucinus subadult male staring at and making protruded lips face toward adult female approaching on the ground. Female made no obvious response. Photo taken at Curt Freese's study site in dry forest at Santa Rosa National Park, Costa Rica.

The open-mouth face usually occurs during play in some cebids (Table 4). The mouth is open, the corners are partially retracted, but the teeth are covered by the lips. It is similar to the "relaxed open-mouth face" that has been described by van Hooff (1967) to occur during play.

The open-mouth-bared-teeth face occurs in many of the New World species as a threat display (Table 4). It has been observed in Aotus by Andrew (1963), but not by Moynihan (1964). In Cebus capucinus (Fig. 1) the mouth is open and the lips are pulled back so that the canines are exposed (Oppenheimer, 1968, 1973). This fits in part the "staring open-mouth face" and "staring bared-teeth scream face" of van Hooff (1967). Weigel (1974) has studied the facial expressions of Cebus apella and found that they have an openmouth-bared-teeth face that is silent, one that is accompanied by a "staccato beep," and a baredteeth scream face that may be similar to that described by van Hooff (1967) mentioned above.

Lip smacking is performed by marmosets, tamarins, and cebids during sexual or friendly encounters (Table 4). In Alouatta seniculus it may be performed with tongue protrusions by a female (Neville, 1972b).

Protruded-lips face has been observed in a number of species. In combination with a frown it functions as an aggressive threat in Saguinus geoffroyi (Epple, 1967). In the Cebidae (Fig. 2) it is a friendly gesture that promotes contact and may be used by an adult male when approaching or being approached by an adult female (Oppenheimer, 1968, 1973). Van Hooff (1967) has also observed this face in an Old World species (Macaca nemistrina) when a male approached a female in heat.

Tongue protrusion is used most often during sexual or friendly encounters to promote contact, though in other species it is reported to be a defensive threat (Table 4). It may accompany lip smacking, and the tongue may either be extended and held out as a single protrusion or be rhythmically flicked, i.e., repeated protrusion. It occurs in marmosets, tamarins, and cebids. In Alouatta villosa the male and female display repeated tongue protrusions toward each other (Fig. 3), which may eventually lead the female to lick the male on the face or body, and finally end in copulation (Carpenter, 1934). In Alouatta seniculus only the female has been observed to protrude the tongue as a single, not repeated, movement (Neville, 1972b). In Saguinus geoffroyi the tongue may be protruded and held in one position, or moved up and down, and with lower motivation it may be moved in and out. It may be accompanied by wrinkling of the nose, partial closure of the eyes, and head flicks. It tends to be primarily a male behavior pattern, used with sniffing in an encounter with a stranger, and during copulation, at which time it may be performed by the female as well (Moynihan, 1970). The behavior suggests that in some species the tongue performs some olfactory or taste function under these circumstances, or at least that the visual display has been ritualized from tasting behavior.

Fig. 3. Howler monkey (Alouatta villosa) adult male, partially suspended by tail, making rhythmic tongue protrusions at female. Photo taken on Barro Colorado Island.

Raising and lowering of the eyebrows has been noted in a number of species (Table 4). Usually the eyebrows are lowered in threat (Fig. 1), but in Cebus apella the eyebrows and forehead are raised during open-mouth-bared-teeth face, which is a threat, and the forehead may be raised briefly with the mouth closed as a submissive gesture (Weigel, 1974). Lowering of the eyebrows is also done while searching for an object or as a protective response (Andrew, 1963).

Partial or complete closure of the eyes is also part of the protective response (Andrew, 1963), and it may indicate submissiveness when an individual is alarmed by some general danger or a threat (Table 4).

Another aspect of the protective response in most mammals is flattening or pulling back of the ears or ear tufts (Andrew, 1963), and it is interpreted as being part of the defensive threat display in some of the New World primates (Table 4).

PELAGE MARKINGS

A fourth type of visual communication has been reported for C. capucinus (Oppenheimer, 1969a). It involves pelage markings or differences on the forehead that indicate the age and sex of the individual (Fig. 1). These signals may be similar to dimorphic differences in body size and shape, size of canines, or shape of the genitalia, all of which remain the same for long periods and change gradually during the lifetime of the individual, but allow rapid recognition of status or potential status even between strangers.

Acoustic Communication

Vocal communication plus some nonvocal sounds like tooth grinding are included in Table 5. Other sounds that accompany visual displays, such as branch shaking, are ignored here. Since each researcher has used his or her own set of names for vocalizations of the species they studied, I have arranged the vocalizations according to the general situation in which they were elicited. The motivation for calls given in one situation by different species may also be different. Thus, I have used the name of the vocalization for each species as used in the literature by the individual investigators. Use of the same name by different investigators, such as "twitter," does not mean that the calls are necessarily the same in physical structure, nor that they are homologous, though they may be. I have tried to come up with a set of generalized circumstances that would fit most calls; however, in doing so some information has been lost and I may have placed some vocalizations in inappropriate categories (a question mark has been inserted where entries were most likely to be wrong). Thus, Table 5 only indicates in what situations New World primates emit vocalizations and which calls of thedifferent species may have similar functions.

Sonograms, such as in Fig. 4, have been made of the vocalizations of a number of species (Andrew, 1963; Baldwin and Baldwin, 1976; Eisenberg, 1976; Eisenberg and Kuehn, 1966; Epple, 1968; Moynihan, 1964, 1966, 1970; Oppenheimer, 1968, 1973; Ploog, 1967; Winter, 1972; Winter et al., 1966), but the vocalizations of other species are just now being analyzed or are yet to be done. Thus, although information is available in part, I will not attempt to discuss the physical structures of the calls in a thorough way. For discussion of the physical structure of primate calls see Marler (1965); however, it should be mentioned that ultrasonic calls do occur, particularly in the marmosets (Epple, 1975).

One needs to be cautious in comparing species studied by different investigators. I have included in Table 5 two studies of the vocal system of Saguinus geoffroyi, one by Epple (1968) and one by Moynihan (1970). Differences in terminology and in vocal situations occurred, and Moynihan has discussed the areas of agreement and disagreement with both Epple and Andrew (1963). Other differences tend to be subjective, for instance "Muckenhirn (1967) . . . reports that wild Saguinus o. geoffroyi are highly vocal while Moynihan (1970) points out that they are actually quite silent" (Epple, 1975).

The vocal systems of the New World primates differ in a number of more specific ways. The simplest is the number of vocalizations: Aotus trivirgatus has 10 (Moynihan, 1964); Ateles geoffroyihas 16, of which 10 are heard frequently (Eisenberg and Kuehn, 1966); Alouatta villosa has 20 (Altmann, 1959); and Saimiri sciureus has 26 (Winter et al., 1966). Possibly with additional observations more call types will be found for species that now appear to have a low number. Another difference is that some species have discrete vocal systems, where each call is distinct and is elicited by specific stimuli, as in Aotus trivirgatus (Moynihan, 1967). In other species the vocalizations may be variable in form, as in Callimico goeldii (Epple, 1968), or may grade into one another by way of frequent vocalizations of intermediate type, as in Callicebus moloch (Moynihan, 1966, 1967). Such differences may also occur between populations of the same species, as in Saimiri sciureus, where the Gothic race has a more discrete vocal system than does the Roman (Winter, 1969b). Even within one species one part of the vocal system may be discrete and another graded, as in S. sciureus (Winter, 1969a) and C. capucinus (Oppenheimer, 1968); in C. jacchus the vocalizations of the infant are more variable than those of the adult, and the infant system seems to be graded (Epple, 1968, 1975). Also some species may combine two vocalizations to make up a third, as in Cebus and Saimiri (Oppenheimer, 1968, 1973; Winter et al., 1966), or may combine two or more vocalizations into a sequence, as in the bark-roar-oodle of A. villosa (Altmann, 1959), the dawn song and gobbling phrases of C. moloch (Moynihan, 1966), and the long call ending in a "coda" of A. fusciceps or the roaring whoop of A. geoffroyi (Eisenberg, 1976).

Calling at dawn or at the initiation of a rain or thunderstorm has been reported for a number of species (Table 5). In A. geoffroyi the call is given with the onset of a storm and acts as a group cohesion call (Eisenberg, 1976). In the other three species mentioned in Table 5, plus Saguinus midas (Thorington, 1968b), the calls are given at dawn, but A. villosa also calls at the initiation of storms or at airplanes flying overhead. In all four species the calls act as an intertroop spacing mechanism. Chivers (1969) has made a detailed study of the dawn calls of A. villosa on Barro Colorado Island, and his data suggest that the daily movements of a troop are set in relation to the location of neighboring troops established at the time of the dawn chorus.

Six species, including the four above that give a dawn chorus, use their long loud call when interacting with another troop nearby or in sight (Table 5). In this capacity the vocalization also functions as an intertroop spacing mechanism, one that uses considerably less energy than chasing and/or fighting.

Most of the New World species have a vocalization that is used when one or more individuals are separated from the rest of their troop. The same call may be used when the troop responds to the call of the lost individual. As in S. geoffroyi, some species may use the same vocalization for a lost call as they use for the intertroop spacing call (Table 5). These vocalizations are usually given in bouts of one to six calls: S. geoffroyi, one to three (Epple, 1968); A. trivirgatus, two to three (Moynihan, 1964); C. capucinus: on Barro Colorado, one to five with an average of three (Oppenheimer, 1968, 1973), and at Santa Rosa National Park in Costa Rica, an average of two (Curtis Freese, pers. comm.); C. nigrivittatus, one to six with an average of 3.2 (Oppenheimer and Oppenheimer, 1973); A. villosa, one to five calls (Baldwin and Baldwin, 1973a); A. geoffroyi, three times; and A. fusciceps, four to five times per bout (Eisenberg, 1976). The use of a number of calls per bout as well as repeated bouts probably help the receiver determine the location of the caller and possibly the caller's identity. For instance, a young capuchin that calls just a few trees away from the troop does not elicit any response, nor do the calls of a nontroop member (Oppenheimer, 1968, and unpublished data). Thus, the long loud calls of each species have the potential to serve as both intratroop cohesion calls and intertroop spacing calls, and in some species they do (Table 5).

The intertroop spacing calls or dawn calls and the lost calls of the platyrrhine species may all have arisen from a similar call of a common ancestor, as they are similar in physical structure, or possibly this similarity was brought about by convergence. The top row in Fig. 4 shows a single "arrawh" call (for comparison with the Ateles call below) and an "arrawh" triplet bout for C. capucinus, as well asthe calls given by a captive C. apella in response to the "arrawh." In the second row only the second call of an Ateles triplet is shown, and these calls were given by the male in order to call the other troop members to him. The Ateles call is twice as long as that of C. capucinus, and it has two narrow-frequency bands instead of the one in the Cebus arrawh; however, it did sound similar to the arrawh. The Alouatta call was recorded on Barro Colorado Island from a captive male who was responding to the roars of a nearby troop. Most of the first and third, and all of the second call of the howler triplet bout are shown, and they are about the same length as those of C. capucinus. Most of the energy is in two frequency bands as in Ateles. The Saguinus contact call was also recorded from a captive individual. The frequency range is much higher and the energy is in five frequency bands, rather than one or two. The higher pitch correlates with the smaller body size of the species (Tembrock, 1963), but Moynihan (1970) also suggests that in smaller species, where danger is greatest from predators, there may have been selection for the higher frequencies, which do not travel as far as the low ones. The sonogram at the left shows parts of three calls from a triplet bout, and it can be seen that the calls are only slightly longer in duration than those of C. capucinus. The sonogram at the bottom right shows a complete call. The C. apella sonogram shows two complete calls and parts of two others. They are shorter than in the other species and show more modulation. They show a greater resemblance to the C. capucinus "huh" call, which is a lower-intensity "arrawh." If this sonogram is representative of the C. apella lost calls, it may be that this atypical call has been selected for because of sympatry with at least one other species of the genus in much of the northern part of its geographic range. Except for the C. apella call, these intratroop cohesion calls and intertroop spacing calls are similar in structure to the long-distance contact call of the timber wolf (Canis lupus: Theberge and Falls, 1967). This suggests that the similarity of function of these calls, to communicate over long distances, is responsible for the similarity in physical structure (Oppenheimer, 1968). For other factors that may influence the physical structure of calls see Marler (1965).

A number of species have a medium-intensity contact call that is elicited as the other troop members move out of sight or when the movement of the caller is blocked by a gap that cannot easily be jumped. In young C. capucinus the "huh" call may grade into "arrawh" calls if visual contact is lost and/or assistance is slow in coming (Oppenheimer, 1968, 1973). It looks as though this may also be true for S. geoffroyi and A. villosa (Table 5).

Most of the species seem to have a contact call that is emitted while in visual contact with other troop members. It probably functions to maintain contact as well as a minimal spacing between members of the troop. This may also be true of the troop feeding call. This call occurs in captives at feeding time or when the human who does the feeding approaches, and in free-ranging capuchins it usually occurs at fruit trees where several individuals feed at once. The call may also draw nearby troop members to the food source (Oppenheimer, 1968, 1973).

A number of vocalizations are given in response to the return of or calls from a separated troop member. In part this may have to do with the particular individual involved, his distance from the troop, the length of the separation period, or the mood of the other troop members.

Table 5

Acoustic Communication

Fig. 4. Sonograms of intratroop cohesion or "lost" calls and/or intertroop spacing calls of five New World species. All recordings made on Barro Colorado Island: C. capucinus and A. geoffroyi calls from free-living individuals, the remainder from captives.

Only in species that have more than one adult female in the troop are the infants reported to emit contact calls when moving on or near their mothers (Table 5). If this is a true difference it suggests that the call functions to identify the infant to the mother when she may not be paying specific attention, as there should also be visual and olfactory cues. In the monogamous species there would usually be a maximum of two infants and they would belong to the same mother.

A contact call given while in physical contact has only been reported from cebid species. These calls are frequently of very low volume, and thus they may have been overlooked in the Callitrichidae, which are all small species (Table 1). Although one might assume that all these calls would be friendly in nature and would tend to prolong contact, this may not be true for S. sciureus. In this species the infant gives milk purrs to its mother while nursing, and adults may give purrs during a genital display, while huddling, or during interruptions in play. Winter et al. (1966) have concluded that it indicates an aggressive motivation. Additional data to support this conclusion would be most welcome, but apparently the social structure of Saimiri troops places a great deal of emphasis on aggressive interactions.

Infants of most species emit calls when they approach their mother to nurse or to be groomed, or when they approach any individual who might give them a ride or some food. These calls most likely promote contact and elicit the appropriate response from the individual approached. Although again in Saimiri the call is supposed to have a slightly aggressive motivation (see above).

Subordinates in most species are reported to emit calls when approaching a dominant animal. In C. capucinus these calls are given by an infant or juvenile who is approaching an adult male. The call is accompanied by head shaking, grins, and a frown. The male makes no response (Oppenheimer, 1968, 1973). The "meow-whine" of A. seniculus is given by a female in estrus when she approaches an adult male (Neville, 1972b). These calls identify the caller as being duly submissive and should appease any aggressive tendencies in the dominant animal.

In fewer species the dominant animal emits a call when approaching a subordinate. Such vocalizations are reported for five species (Table 5). The vocalizations used are contact or greeting calls, except for the two species of Saimiri, which have in addition a call specifically for this purpose. It is interesting to note that the Saimiri species seem not to have a call given by a subordinate to a dominant animal (possibly this is due to an error on my part in interpreting the literature).

Only two species are noted to use a call when individuals approach a peer (Table 5). This is probably because the category is too general and such encounters occur under specific conditions, such as play and grooming. Nonetheless, it may be that there is less need for peers to communicate with one another in the vocal channel.

Play, particularly easy play, seems to be silent in most species. In the three species that are reported to vocalize during easy play, primarily contact calls are used. In rough play the vocalizations tend to be alarm or fear calls that may elicit assistance from other troop members and/or terminate the play interaction, at least for the moment.

Thwarted approaches occur when the approacher has a strong motivation to approach and is prevented from doing so by the approachee. In capuchins this occurs during the weaning period when the infant tries to nurse or to ride on its mother. The rejected infant gives contact twitters, distress trills, and tail-rump waggles (Oppenheimer, 1968, 1973). In C. goeldi when an estrous female rejects a male the male makes "a sharp smacking noise with his teeth (or tongue) . . ." (Lorenz, 1972).

Though in all species males must approach estrous females, vocalizations are reported to occur during these encounters only in the Cebidae. These calls on the part of the male seem to have an appeasement function and should encourage contact. The "ook ook" call of A. geoffroyi is given by males in captivity when approaching an estrous female (Eisenberg and Kuehn, 1966), but Klein and Klein (1971) say that in the wild this call is part of play behavior.

In all species, individuals respond to threats with vocalizations, and most species have more than one type of vocalization. The different vocalizations are usually keyed to the intensity of the threat, though the threshold levels are yet to be established for some species. The response to the most intense threat is in most species a scream, screech, or squeal.

It is usually the scream or other vocalization used to respond to intense threat that is used to elicit assistance from a third party. This call may be given even though the caller has received only a mild threat or none at all, as when an adult female capuchin approaches a human observer long after visual contact has been made (Oppenheimer and Oppenheimer, 1973). Thus there may be a certain amount of flexibility in the amount of stimulus needed to elicit the call. An individual easily excited may respond with a scream even though the stimulus is of a low level, and/or an individual may scream in order to obtain positive feedback from the assisting individual.

In many species the intraspecific threats, which may be primarily visual (also olfactory andtactile), are accompanied by vocalizations or other soundslike tooth grinding and gnashing. In the Callitrichidae the intraspecific threat vocalizations may be the same as those used to mob another species or to alert the troop to the presence of a predator. In C. capucinus the only threatening sound is that of tooth grinding, and it is used only in intertroopor interspecific (at human) encounters (Oppenheimer, 1973). In Saimiri and Ateles, the two mostaggressive species, there are clearly three levels of vocal threats (Table 5).

General alarm calls are reported for a number of species. These calls may be the same as a vocalization given in response to a mild threat or a contact call, or they may be specialized calls.

Mobbing calls are elicited by snakes or other terrestrial animals and are given by several troop members. In the Callitrichidae the mobbing calls are different from the alarm calls (Muckenhirn, 1966), whereas in the Cebidae the mobbing and alarm calls may be the same (Table 5).

The alarm vocalizations elicited by terrestrial animals and birds flying overhead are usually the same; however, there may be temporal differences. For instance in C. capucinus and C. nigrivittatus the "grrah" is repeated by an individual many times when the stimulus is a terrestrial animal, but it is given only once to a bird overhead (Oppenheimer, 1968, 1973; Oppenheimer and Oppenheimer, 1973). Although the vocal repertoires for many species are incomplete, it is interesting to note that the nocturnally active Aotus and the diurnally active, and large, Alouatta and Ateles have not been reported to give alarm calls to birds overhead. To complete a full circle, the alarm calls of some species (S. geoffroyi C. moloch, Saimiri, A. villosa) are similar to or the same as the vocalizations used by these species as intertroop spacing calls, lost calls, or general contact calls. Epple (1975) and Moynihan (1970) have both heard the lost call during intertroop encounters. Epple states that the vocalization draws the other troop members to the caller and thus serves as a "call for assistance."

Comments

The studies of communication in the New World primates range from cursory observations, with consequently little descriptive information, to detailed studies of a specific behavior pattern. Representative of the latter type of study is the work of Symmes and Newman (1974), where variants of the isolation peep are played back to squirrel monkeys (Saimiri) in order to determine what physical part of the call is functional.

Between these two extremes are the studies that present a complete or partial list or narration of the behavioral patterns of a species. In many cases when motivations or functions are attributed to the behavioral patterns, these determinations have been arrived at on purely subjective grounds. Listing and describing behavior patterns are certainly basic and necessary steps toward understanding how the New World primates communicate, but they are only the beginning. What we need to do now is to determine quantitatively the relationships between the various behavior patterns of a species, as has been started for Saimiri (Winter, 1968), Cebus (Oppenheimer and Oppenheimer, 1973), and Ateles (Eisenberg, 1976). Such an analysis provides a more objective method for determining motivation and function. Once these studies are completed the structure of primate communication systems (or ethograms) can be compared among related species, as well as among the different genera. Such comparisons will yield a much greater understanding of communicatory behavior and of the evolution of such behavior than do comparisons of individual behavior units of a number of species, as have been presented here.

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