Vocal communication in New World monkeys

Many feature5 of thr vocal rwnmunication s~stcms ofNew LVorld primatr,s

are similar to the most complrx vocal s)stcms known: human sprrch ;md

bird Sony. This paper wvirws the parall& between vocal communicalion

in New M’orld monkeys and phrnomrna of bird song and human spwch.

The long or loud rails of Nr\v World monkeys are functionally similar ((I

bird song, being used for maintaining trrritories, for intraqroup cohesion

and for mate attraction. These long calls have features that allou Ior

species, suhspecics and individual recognition. While the long and loud

calls ofsome New \Vorld primates fit thr design features that maximizr Irmy

distance transmission in tropical hahitats, the long calls ofmost callitrichid~

are pitched too hiqh li)r maGnal distanrr of transmission. Thert. i,rx’

parallels in the ontogen! of hird sting ;md thr ontogen! of Ion!: c,~Il\. \

highly \wiahlc XI ofcalls is urcd hy imm~~urr animals cr!stallizin,< inil, o

stewott pcd form with rcproducti\,r maturation. Thaw iy ~‘1 idcncv 01

phonc& uriation \vith catc,gorical perception of dilliererent calls in p!ym\

marmosets. A rudimentarv svntau and orduly turn taking hrhaviol- h;l\c been found in many New \<orld primates. 1; squirrel monkeys thcrr is evidence of a metacommunicative function of calls. The vocal communica- tion systems of New World monkeys represent some of the most sophisticatrd \ncal qstcms liwnd in nrmhuman primates.

introduction

Students of?l:ew World primates have long labored under an inferiority complex. Lt’c ha\,c

allowed our colleagues who study Old World primates or apes to convince the scientific

community that their work is more valuable because their species ha1.c greater

phylogenttic relatedness to human beings than New World primates. Perhaps nowhere

else are the evolutionary accomplishments ofNew FVorld primates so clearly dominant as

in their communicative abilities. Most ofour current understanding of the use ofolfactor)

communication in primates comes from studies of New World primates, mainI>, the

callitrichids (Epple, 1986). Many of the currently interesting phenomena of vocal

communication are found in New World primates.

This chapter focuses on vocal communication. There are two models of complex

communication that will be used to organize the results. The first is human speech and

language; the second is bird song. Both have been studied extensively, with bird song often

used as a model of human speech (Marler, 1970). 0 ur k nowledge of bird song and speech

has bern used to generate a set of research questions that can bc asked of New U’orld

primates. While analogies from birds and human beings are useful guides to asking

questions of New World primate communication, I shall also argue that findings from the

stud?, of New World primates lead to interesting questions to ask about human sprech and

about bird song.

First, I will consider some of the methodological issues involved in studying primate

communication. Then I use the loud or long calls of New World primates as a model

\rocalization analogous to bird song and examine the parallels to bird son\g in studies

related to the structure ofcalls as an index ofspecies, subspecies, individual and contestual

0(147-L’-IH4it19/070t) I I + 23 $03.00/0 @ I989 Academic Press Limited

612 c:. ‘I‘. SNo~vnoS

differences; the design features of the calls that allow long distance transmission and rc,ad\

localization of the signaller, and finally the ontogeny of these calls. Nest I consider

affiliative or contact calls which displav many resemblances to phenomena of human

communication, using the trills of pygmy marmosets and the isolation peeps and chuck

vocalizations ofsquirrel monkeys as model systems. I then look at the function of\zariations

in call structure, how call structure is adapted to the environment, the way in which these

calls are perceived by monkeys, individual variation in structure and usage ofcalls. and the

ontogeny ofaffiliative and contact calls. Finally I consider some esamples ofmore cornpI&

communication-the organization of calls into structured sequences according to a

rudimentary grammar, the organization of calling between members within a group and

between groups.

Methodology

Before any analyses of complex vocal communication can be made, it is essential to have a

good natural history of vocal communication. This natural history can be obtained from

two sources. The most obvious source is in the wild where one can observe all of the

potential contexts associated with vocalization. However, it is often difficult to get close

enough to the animals to obtain good recordings of softer intragroup vocalizations in the

field. Thus, field studies are often biased toward loud and conspicuous vocalizations

(although there are some important exceptions where relatively quiet intragroup

vocalizations have been recorded; see Robinson, 1982; Snowdon & Hodun, 1981).

In a captive environment one can identify calls with precision, recording every

vocalization regardless of amplitude, and one can be relatively certain of which individual

is calling. Experimental manipulations to study how monkeys respond to vocalizations and

how they perceive their own calls are often simpler with captive populations. Thus there

are many research questions that are best answered in captive populations. In order for

studies in captivity to have any validity, the animals must be housed in social groups that

approximate those found in the wild, and they should be provided with an environment

sufficiently large and complex in which to express the range of vocalizations that would be

likely to occur in nature. However, no captive environment can approach the complexity of

the natural habitat, so the best solution for determining the vocal repertoire ofa species and

studying the communication system in all its complexity would require moving back and

forth between field and captive studies. Unfortunately, few investigators have studied the

same species in both environments.

Once one has obtained an understanding of the types of calls given and the contexts in

which they generally occur, the next step is to classify the vocal repertoire into basic vocal

units. In an ideal world these units should be sortable into categories that could be related

to specific contexts. The reality is often more difficult. Various techniques have been

proposed to attempt a classification. Cleveland & Snowdon (1982) sorted short,

frequency-modulated calls (chirps) of-cotton top tamarins (Saguirm o. Oedipus) according to

the context in which they occurred and then made quantitative measurements of several

parameters of the calls. They analyzed these parameters as a function ofcontext, and found

that different structures could be associated with different contexts. Goedeking (1983) has

developed a computer program for extracting distinctive features from cotton top tamarin

calls to sort calls into classes. Other investigators have simply used visual inspection of

sound spectrograms to develop call categories.

VOCAL COMMI.NICATIOh’ IN NEW 1~ORI.D MONKEYS 61 3

Each of these techniques creates a problem. All sorting schemes are ultimately based on

the perceptual abilities of the human investigator or inferences from a human perceptual

system built into a computer program. These may not be isomorphic with the perceptual

system of the monkeys. An idea1 study requires that tentative call categories should br

tested in perceptual studies with monkeys.

As an example of one such test, Bauers & Snowdon (in preparation) studied tht’

discrimination of two chirp variants of cotton top tamarins, the F-chirp and G-chirp (SW

Cleveland & Snowdon, 1982). These two chirps were similar in acoustic structure.

differing only in the start frequency and frequency range. However, these calls were used in

two diKerent behavioral contexts and led to different responses in spontaneous usage. ‘1’11~

Fchirp is given frequently in territorial encounters, when the sounds of a strange group

have become audible. The G-chirp is given in relaxed conditions appearing to scrvc’ as a

contact or location call. Examples of each t),pe of chirp recorded from an unfamiliar

monkey were presented in a playback test to eight captive groups of cotton-top tamarins.

The behavior and vocalizations ofthese tamarins were recorded both prior to and following

the stimulus presentation. Both stimuli elicited alerting responses, indicating that each was

tleing attended to. However, the F-chirp led to increased activity, freezing, scanning and

pilorrection and an increase of F-chirps, Squeaks and Flat Whistles (calls indicati1.e 01‘

arousal). No changes in behavior occurred foltowinLg the presentation of the G-chirp. ‘1%~

differences in response to the two types of chirps were apparent even on the very first trial.

‘I‘he animals discriminated the chirps even though they were only 75 ms in duration and

\vcre quite similar in acoustic structure. The animals responded with the same beha\rioral

pattterns that the)- would have shown following a spontaneous emission of each call.

indicating that there was enough information in the call structure itself to lead to 21

scmanticall~- appropriate response in the absence of all othrr contextual cues.

This playback technique is a very powerful tool fi)r studying perception of calls, fi)r

developing an understanding of the function ofdifferent calls and for analyzing some of the

acoustic variables important in call transmission. The technique has been widely used not

only in our laboratory, but by other investigators working with captive populations and in

the field (Masataka, 1983; Symmes & Biben, 1985; Masataka & Symmes, 1986; Htarzog &

HopI; 1984; IVhitehead, 1987: Robinson, 1979. 1984).

Parallels with bird song

Functional similarities

The long calls or loud calls of New World primates show many functional and structural

similarities to bird song. Moynihan (1970) suggested that tamarin long calls are used to

maintain distance between neighboring groups, to promote cohesion within a group, to

reunite group members which become separated from one another, and in mate attraction.

There is no difference between these functions and those suggested for bird song.

Structurally the long or loud calls show resemblance to bird song. The calls are typically

much longer in duration and much louder than vocalizations used in other contexts. They

generally consist of several notes or syllables that are repeated over a time course of several

seconds. The notes are conspicuous, containing features that make the caller quite easil)

detected by others.

Probably the most conspicuous and best known of these types of calls arc the roars of

howler monkeys. Sckulic (1982) f ound that 95% of the howls given by red howler monkeys

61-l (1. '1'. SNO\VI~ON

(.4louattu seniculus) were directed to\vard solitar!, individuals and mc~mbers ~t‘nt~igl~l~~t~itl~

troops. Sekufic suggests that mates evaluate conspccilic howling to assess their opponents

and thereb), avoid serious fights and cflases. Howls appear to rrfjef solitary males and

subordinate males in neighboring troops that may attempt to rcplact* the resident malt’.

In Old World primates almost all long or loud calls arc given onI>- by males. but SC\\

World primates are more egalitarian. Female howler monkeys howl both at females tiiom

other groups and at other males (Sckufic, 1983). In the latter casr females sit near the

resident males, suggesting that female howling is used to strengthen the pair bond betMccn

male and female and to incite competition among males.

In the monogamous titi monkey (Callicebus moloch) Robinson (1979, 1981) found that

both sexes give loud calls in duets. Early in the morning males often call alone near the

boundaries of territories, but separated from other groups by at least 100 m. This elicits

calling from neighboring groups. Both groups approach the boundary, with each femalc

staying close to its mate. Duetting begins when both mates arc in close proximit) and

continues until both groups arc within 30 m of the boundary. Then other calls are used.

After these morning cncountcrs the groups retreat to the center of their home ranges.

Robinson suggests that the long calls and duetting of Cdlicebus moloch are used to define and

reinforce territorial boundaries, decreasing the likelihood ofintertroop encounters at other

times of the dav. He also suggests that the duetting serves to reinforce the pair bond.

Kinzey & Robinson (1983) found different responses in Cullicebus toryuatus. Playbacks of

the recordings of adult mates fed the group to flee from the site of the recording rather than

approach it. When duets were placed back, on the other hand, the group stopped and

counter-catted with the playback duet. The ductting and male loud calling in c’. toryuatuJ

appears to maintain spacing between groups while minimizing all hut \,ocal interactions

between groups. The homologous calls in c’. moloch define and reinforce the houndar)-

location. The net result is similar, howcvcr; the maintenance of spacing between groups.

Neyman (1977) reported that cotton-top tamarin long calls arc used during intertroop

encounters between animals which occurred about twice a week and were accompanied b)-

a variety of other vocalizations. McConnell & Snowdon (1986) developed a capti1.e

simulation of territorial encounters in cotton top tamarins. IFdoors were left open betw~~cn

diKerent rooms in a colony the normal intratroop calls of’ unfamiliar groups w-ere heard

with increased intensity, similar to what would f,e heard if two groups approached each

other in the field. I‘he tamarins did not respond to the changes in vocalizations until aflout

30s elapsed, when one or more animals would orient toward the sounds and then start a

tong calf bout. For the next several minutes there was great vocal activity among the adults.

A variety of calls including tong calls and F-chirps (see above and Cleveland & Snowdon,

1982) were given. Females gave long calls more frequently, while males gave more F-chirps

and repeated trills of F-chirps. There was also an increase in behavior associated bvith

aggression or group defense such as increased activity, increased scent markin,y and

piloerection, and increased scanning. Thus, long calls are used extensively when groups

can hear the approach of a neighboring group, and may be used as a means of maintaining

intergroup spacing. In subsequent studies McConnell 6i Snowdon (unpublished observations) separated

individuals of mated pairs from one another for brief periods of time ( 1 11). They Ibund an

immediate increase in long calling which was maintained for the duration of the

separation. Thurwachter & Snowdon (unpublished observations) also lbund thatju\~enile

tamarins separated from their groups gavejuvenile Forms of the long call. They produced

VOCAL COMMUNICATION IN NEW WORLD MONKEYS 6 I ,Fl

as many as 30 different variations in a 50 min separation. Thus in tamarins, as with titi

monkeys and red howlers, long or loud calls appear to be used for territorial defense,

intergroup spacing, and intragroup cohesion. These functions are similar to those reported

for bird song (Kroodsma & Miller, 1982).

cStructural rimilarities to bird song

L’ariation in acoustic structure in bird song has been linked to taxonomy. species

identification, subspecies identification, individual recognition, social context and

n1asimizin.c transmission of sound through the environment (see Kroodsma & Miller.

1982). In tamarins, long calls display a \.ariety of structural differences which can bc

related to their taxonomy, geographical distribution, individual variation, social context

and environmental context. In most species of callitrichids, the long calls consist of a long

series of short. frequency modulated notes that are relatively high-pitched (5-8 kHz) (see

Figures l-3). The only exceptions found so far are the two species occurring in

northwestern South America, the cotton-top tamarin (Sag&us Oedipus) and Geoffroy’s

tamarin (Saguinus geojjkyi). In these species the long calls consist of two or three relativcl),

low-pitched (2-3 kHz) whistle-like calls with little frequency modulation (C:leveland &

Snowdon, 1982; Muckenhirn, 1967) (F’g I ure 4). It is somewhat puzzling why these two

species should have long calls that are quite different in structure from all the others.

Although most callitrichids have short. high-pitched, frequency modulated notes in the

long call, the variation in long call structure permits taxonomic identification. The location

A

1 -L+&-r----- -

B

D

1 I 0 0.5 1.0

Seconds

Figure 1. Sound spectrograms of long calls of four subspecies of the saddlehacked tamarin, Saguinus

Jwicotlis. A, S.j.fuscicollis; B, S.f. illigeu: C, amalgam of S.jI iltigert and S.J nQ+fions: D. .S.j nig~~~onx E. S.,fi fqontus. (from Hodun et al.. 1981).

616 c:, I‘. SS(~\VL)OS

16 r Leonioplthecus chrysomeios CPRJ

16 Leontoplthecus chrysopygus CPRJ

12 r4 t fi8 _ _ _ ._ . . -.

_.~__ _,____--_-_-_--- c

0

16 Leontopithecus rosalm CPRJ

_ \ 12

z8 4 --_- __A__ .-w----S--. /-r; -_

16 r- Leontoplthecus rosal~o Monkey Jungle

12

:a 4 1

_-I-c* -n--x ----_ -----.

OW I .o Seconds

Figure 2. Sound spectrograms oflong calls ofdill’erent species oflion tamarins, Leonfopilhcru~, recorded at the Centro de Primatologia do Rio de ,Janeiro (CPR,J-FEEMA) or Monk?? ,Jun~lr. Florida il’r~~~ Snowdon et al.. 1986).

of the frequency modulated portion of the note, the degree of frequency modulation, the

relative timing of peak frequencies and relative pitch of different portions of the note all

contribute to taxonomic distinction in call structures. Hodun el al. (1981) found clear

differences in long call structure in four subspecies of the saddle-backed tamarin ( bSuguinuJ

fuscicollis), especially among the three subspecies whose ranges abutted one another. One

subspecies (S. jI illigeri) had consistently shorter notes than all of the others; another (S. ,/I

fuscicollis) had much less frequency modulation in its notes than the others: the third (,S.,/: nigrifrons) had both longer notes and notes with frequency modulation (Figure 1).

A similar problem exists among the lion tamarins (Leonto@~cus), which consist of thrct.

separate species, each with a species-typical form of long call. Snowdon ef al. (1986)

recorded long calls from all three species (Figure 2) and found that the golden-headed lion

tamarin (L. chrysomelas) had shorter notes and higher pitched calls compared to both the

golden lion tamarin (L. rosalia) and the black lion tamarin (L. chyvsoivgus). The golden lion

tamarin was intermediate to the other two spccics in several call paramrtcrs. ‘I’hc

differences in vocal structure closely paralleled differences in craniodental morphology and

fit with the pattern of geographical distribution of the three specirs (Rosenbergrr &

Coimbra-Filho, 1984). Thus, vocal characters of long calls can be used to c~mpleme~~t

traditional taxonomic analyses.

One would predict individual differences must be present in long call structure. An

animal must alter its response according to the degree of familiarity with the caller and

according to context (e.g., a cohesive context or a territorial context). ‘IIese asprcts ha\,c

been studied in a. number of ways. Snowdon 8r Hodun (1985) studied the responses of

newly captured troops of the mustached tamarin (Suguinus mp.rfus) to the temporarv

separation of a troop member. An attempt was made to capture entire. intact troops. ‘1%~

VOCAL COMMUNICATION IN NEW WORLD MONKEYS 617

19 -6

19-Z

0’

I .O second

I‘iguw 3. Sound spectro,qrams of long calls fr~~rn individual mustached tamarins. Squinuc vy!frr\, wwrded \\hik the! near srparated from thrir troop (from Snowdon & Hodun. 198.5).

individuals in each troop were housed in separate, contiguous cages. In the experiment an

animal was removed from the troop cluster and placed out ofvisual contact with the rest 01

its troop. It soon began to give long calls (Figure 3). The vast majority of responses to a

separated individual came from that individual’s own troop even though many other

individuals from other troops were nearby. The long calling of an isolated tamarin did not

elevate the general arousal level of all tamarins within earshot, but rather its long calls

specifically aroused members of the animal’s own troop. This indicates that individual

troop members can be recognized on the basis of vocal information alone.

Snowdon it al. ( 1983) considered the effects ofboth individual differences and contextual differences on call structure and on call response in cotton-top tamarms. They recorded the

spontaneous long calls of individual tamarins given in territorial calling and in the context

of cohesion long calling, the Normal Long Call and Quiet Long Call, respectively (Figurr

4). Several parameters of call structure were analyzed, usin,q discriminant function

618 c:. .I‘. YNO\VI~OT\

techniques: 98% of the long calls were identified correcti). pro\+Ilg that the c,itls usc~l irl different contexts have distinctly different structures. ‘I‘hc discriminant anal~scs also detected individual calls at a significantly higher rate than predicted h>. chance. Some, individuals had highly distincti\.c calls that could bc disccrncd at nearly pet-f&t Ir\.cls, while other animals wcrc less distinctive. Animals were tcstcd using a playback paradigm. Tamarins responded more to the calls ofunfamiliar than to familiar animals, and they ga\‘t’ different responses to the Normal Long C:atls and the Quiet Long Calls. They showed aggressive responses (piloerection, scent marking) to the territorial long call. and alarm

responses to the intragroup cohesive call. This latter result is, at first glance, surprising. However, since the animals were being exposed to the normal intratroop call of a strange individual, and it would be rare that such a stranger would <get close enough to a troop to give this call without arousing a territorial dispute, it is evident why the group responded to the intragroup call of a stranger with alarm. Playbacks of intragroup long calls from the

animal’s own group elicited no responses.

Normal long call 16

12

4 I N 0

’ 16-

12

8~

4-

O-

Quiet long call

__

1 *ik,.

Comblnotlon long call

_.-- -- _.z.

0 0.5 Set

Figure 4. Sound spectrograms of three types of long calls from the cotton-top tamarin. Snguinu~ opdipus. Normal Long Calls are given during intergroup encounters. Quiet Long Galls are given for intragroup cohesion, and Combination Long Galls arc highly variable forms of long calls given by juveniles and nonreproductive adult animals (from Cleveland & Snowdon, 1982).

Relationship of call structure to environment

There is a growing literature on the relationship between the physical characteristics of signal structure of birds and primates and their habitats (Wiley & Richards, 1978; Wasel & Waser, 1977; Waser & Brown, 1986). It has been argued that loud or long calls should be structured to provide maximum transmission through the environment. If calls serve to repel other groups, then they must travel far enough to be heard by other groups. Within tropical rain forests there appears to be a special low frequency window for maximum acoustic transmission, generally between 500 and 1500 Hz. The structure of the roars of howler monkeys, therefore, is ideal for maximum sound transmission through a rain forest habitat.

Waser & Waser (1977) reported that atmospheric effects influence the transmission of’ loud calls in mangabeys (Cercocebus albigena). Sounds in the frequency range of mangabey (and howler monkey) loud calls traveled further at dawn, less at dusk and least at midday.

VOCAL COMW-NICATION IN NEW WORLD MONhEYS 619

In the African forest where the Wasers worked, the mangabeys gave the most loud calls at

dawn, even though the ambient noise in the environment was greatest then. The LVascrs

sug,qested that thr large temperature gradient between the ground and the canopy which is

found at dawn acts as an acoustic lens that reflects acoustic energy downwards, dccrcasing

acoustic spread through the atmosphere, hut increasing acoustic energy close to the ground

and therefore maximizing the distance travclcd.

Reports on New World primates have indicated that loud or long calling is also most

frequent at dawn (Sekulic, 1982aJ; Robinson, 1979; Kinzcy & Robinson, 1983). An

extension of the \Vaser hypothesis would suggest that on overcast or rainy days thert,

should be little difference in temperature <gradient; thus long calling would not he as

rffec-tive. This appears to be supported by Sekulic (1982~) who showed that red howler

monkeys howled less often during the rainy season, and that the diurnal pattern ofhowline

was less pronounced in the rainy season than in the dry season.

LVhitehead (1987) described another acoustic variable of importance in loud call

transmission : reverberation. As sound travels through the forest, low frequency waves art

scattered by the interferences of various structures located between the source and the

receiver. This leads to greater reverberation in the sound in direct proportion to the

distance between caller and recipient, and offers a mechanism of localization. If a recipient

attended to changes in the reverberation ofcalls, it should be able to determine whether the

calling animal is approaching, retreating or maintaining the same distance. Whitehead

prepared stimulus tapes of two types, the first a clear loud Cal! followed by a reverberated

loud call, which would be the sequence one would hear from a retreating animal. The

second was of a reverberated loud call followed by a clear loud call simulating the cf&ect ot

an animal approaching the receiver. In playback studies involving howler monkeys. males

approached sounds that simulated an approaching male, while they withdrew from sounds

that simulated a withdrawing male. Thus reverberation cues can be used to assess the,

relative direction of movement of another animal.

These stud& point to some generalized rules regarding the ideal structure of primate

long calls. Yet they do not apply to the long calls of most of the callitrichids. Only the long

calls of the cotton top tamarin and Geoffrov’s tamarin approach the ideal frequency for

long distance transmission. The other calli&ichids have much higher pitched calls than

would he predicted if distance of transmission we‘re the major selective advantage. Studies

of sound transmission in tropical rainforests (bl’aser 8r tSaser, 1977: \Vascr 8r Brown.

1986: hjarten PI al., 1977) have shown that excess attenuation exists for such high

liequency sounds. ‘I-hat is, high frequency sounds appear to be reduced in amplitude as

the)- encounter leaves, twigs, trunks, etc., more acutely in rain forests than in temper;rtc~

lijrests. \Vhy then do callitrichids tend to have such high pitched calls?

Snowdon & Hodun ( 1981 ) studied the calls of pygmy marmosets (Cebuella p~yrmw) in

thr Peruvian Amazon and found that they appeared to make use of an acoustic window in

the ambient noise. hlost ofthe pygmy marmoset calls were found above 8 kHz in frcqucnc)

whrrc there was little competing ambient noise. Since callitrichids are small and may have.

smaller territories or home ranges than larger primates, long distance transmission ma\

not be as important for them as it is for howler monkeys. In the absence of any special

adaptations to amplify sounds, and with small body size. a callitrichid ma) be more’

effective in usirlg a high frequency channel that has rclati\,clv little competition from other

species in its environment. Large birds produced the most intense alarm responses hJm

pygmy marmosets. Since few birds, other than such nocturnal predators as owls, ha1.c an

620 (.. ‘I’. SXO\VlX)X

acute hearing capacity beyond 3-6 kHz. the LISC of‘ high pitchrd lorig calls 1)) callitrichidz

may also reflect an anti-predator adaptation. Finall).. the csccss attenuation at high

frequencies provides a distance cue. U’hcn two animals arc close to each other, thy hi+c,ht

frequency components will hc nearI). as audihlc as the lowest frcquenc). components.

However, as the distance between caller and recipient increases, thrrc will be a progrcssi\.c,

fading of the high frequency components. Thus, the frequency modulated, high pitched

long calls of the callitrichids can provide information about the location, distancr and

direction of movement of the caller similar to the rcl,erhcration cues in the ho\vls of howler

monkeys.

Although there are many studies on environmental constraints on communication in

birds and primates, there are no parallel studies on the importance of these factors in

human speech. Here is one area where a study of animal signals can raise interesting

questions about human speech.

Ontogenetic similarities to bird song

Because of the close relationship between structure and function of primate long calls and

bird song, one might expect to see similar ontogenetic mechanisms involved. Since bird

song ontogeny has been used as a model of the ontogeny of human speech (Marler, 1970),

demonstrating parallels between primate avian ontogeny are important to our

understanding of the evolution of human speech. In bird song there is frequently a scnsitivc

period for learning song (Marler, 1970), although this is mediated by the social

environment of a bird. One does not hear adult song until the start of the second year oflife

when the male bird reaches sexual maturity. However, there is a period just preceding the

attainment of adult song when one hears plastic song, a highly variable, immature form 01

singing (Marler & Peters, 1982).

In tamarins, there are parallels to the ontogeny of bird song. Hodun et al. (1981). in a

study of saddleback tamarins, noted one anomalous animal whose long call appeared to be

an amalgam of the calls given by its own subspecies and by the subspecies found dircctl)

across the river within earshot (Figure 1C). Three explanations are suggested for this

amalgam. First, the monkey may have been a hybrid and its long call reflected the

subspecific features of each of its parents. Second, it is possible that if a troop of the other

subspecies was in close proximity during development, the animal may have learned

characteristics of the long calls of both subspecies. Third, the calling pattern of’ its own

subspecies may develop along an ontogcnrtic pathway which includes ajuvenilc stage that

contains the features of adult calls of both subspecies. Hodun et al. (1981) discovered t\vo

captive adult animals which were known to be hybrids of the same two subspccics

examined in the wild. When they recorded and analyzed the long calls of these hyhrids,

they did not find the expected amalgam ofparental call types but did find some features ofa

third, unrelated subspecies which was the dominant subspecies housed in the same room as

the hybrid animals. This provides a strong, but not conclusive, indication that tamarins

might learn their long calls from other animals with whom they interact. The possible hormonal basis for long calling and the existence ol‘a plastic song analog)

are suggested from studies of the cotton-top tamarin. Cleveland & Snowdon (1982)

reported that juvenile and non-reproductive adult animals did not give the adult forms of

Normal and Quiet Long Calls. Instead the), used a high]), \:ariable form of the Iona call

(Figure 4). Subsequently, Snowdon et a/. (1986) found that the rate ofgiving these high]>

variable calls peaked at the age when animals would normally reach puberty. Cotton-top

VOCAL COMMUNICATION IN NECV \VOR LL) MONKEYS 621

tamarins become reproductively functional only under appropriate social conditions.

Reproduction is suppressed in animals li\ring in the prcscncc of sexually mature adults

(French et al.. 1984; Ziegler et al., 1987). H owever, sexual maturity is rapidly attained

(ovulation and conception occurring in as little as 8 days) when animals are removed from

a family group and paired with a mate. There is a close correlation between adult lon,q cxlls

and the individual’s hormonal status. In females, rstro‘gen lc\& rise sharpI?- after animals

arc paired with a mate, and the calls invol\red in territorial drCense, such as the Nolmal 1,011g call, appear for the first time. On rare occasions a sexually immature animal will gi1.t.

a Quiet Long (Iall, the cohesive form, but the rate of Quiet Long Calling increase5 wheII

sexual maturity is achieved. Thus, in the cotton top tamarin, as with many son,q birds.

there is a period of great vocal variahilit\- in loq calling which is transl‘ormed into

stereotyped call structure with the onset of sexual maturit\..

Parallels with human speech phenomena

Scvcral phenomena from human speech ha\.c parallels in \~~a1 communication in Sew

\;l’orld primattts. One characteristic of speech is a phonetic structure where suhtlt

diffrrcnccs in sound structure have difrerent meanings, These phonemes can be combined

10 &x-m words and longer strings of utterances. Many studies sho\%,ed that humarl speech

sounds arc perceived catexgoricall>-. That is, MW ignore 1nuc1~ of‘ the variation in phonytic,

structure when we listen to speech, and wt. hall well-defined perceptual boundaries Ihat

alloy us to make precise discrimination between catc~gories. ‘l’hrrc is evidence ol’simila~

phonetic variation in New \Vorld monkeys with somt’ e\idcnce li)r categorical perceptioll

and the existence of a rudimentary- grammar. In addition, there is csvidence hr. soc.iaI ~IIICY

govc~rnin~g con\~ersations or vocal erchangc~.

r-2

3:

16 - A B

12 -

8 : au-

4-

0

16 l-0 E

Seconds

622 L. ‘I’. SNO\VI)ON

Phonetic variation, categori;ation, and ontogen)

P_vgmy marmoset trdls. The trill vocalizations of pygymy marmosets are brief, sinusoidal,

frequency modulated calls that appear to bc used mainlv in situations ofafliliation. or to

maintain contact between group members. In the wild these calls arc used as animals mo\~

through the home range, when they are often out of sight of one another. Trills are used to

rally animals to the sleeping site at the end of the day, and they are also used by sentinel

animals while other animals are resting or grooming at midday. Close examination ofthese

calls indicated that there were several variants.

Pola & Snowdon (1975) described four variants in pygmy marmoset trills (Figure 5).

The most common trill in captive animals is the Closed Mouth Trill. Similar to this trill in

every dimension except amplitude and the frequency range is the Quiet Trill. The

frequency range of Quiet Trills is l-2 kHz rather than the 3-5 kHz frequency range Ihund

with the Closed Mouth Trill. A third form of trill, the J call ( named after its qualitative

appearance on a sound spectrogram), is an interrupted trill. Only the upsweep ofthe sine

wave is visible, the downsweep is not uttered. These calls are much longer, nearly 1 s in

duration, compared with 150-250 ms for the other calls, and have greater frequency range,

typically 5-6 kHz. The final form of the trill is the Open Mouth Trill. This trill appears to

be identical to the Closed Mouth Trill in all dimensions except duration. Closed Mouth

Trills were always less than 250 ms in duration while Open Mouth Trills were always

longer than 250 ms in our original study. Close examination of the contexts in which the

trills were given failed to show an)- differences in context among the first three variants.

However, the Open Mouth Trill was followed with a high probability by aggressive ot

agonistic behavior, suggesting that it was being used in a different context.

Figure 6. Antiphonal responses to synthesized trills in pygmy marmosets. Note category boundary-

hetween 248 and 257 ms. CMT. Mean duration of spontaneous Closed Mouth Trill. NULL. Response

rate when no stimulus is presented (from Snowdon & Pola, 1978).

VOCAL COMMIINICATION m NEW \\~ORI.D MONKEYS 6213

‘I’his led to the question of possible differential response to playbacks of Closed Mouth

and Open Mouth trills, and to a related question concerning human vocal perception.

When speech sounds are played to human subjects, they discriminate the sounds in a

categorical manner. Thus, if we are presented with a continuum of sounds varying along

the acoustic dimension that contains the phonemes /ba/ and /pa/, we do not prrceive each

different sound as being different, but rather hear many different sounds as being similar

either to /ha/ or to /pa/. Instead of continuous variation we perceive a sharp boundary

between two stimuli that represents the categorization of a continuum into two discrete

units. Do monkeys perceive their sounds in a similar \vay?

40

30

20

IO

: 0 ; 5 d h a 20

IO

5

IO

5

Closed molith trill

1.5 3 6 9 12 15 I8 21 24 34.5

Dlstonce 1 m)

624 c:. ‘I’. SNO\VI)O~

‘I’he trills of pygmy marmosets were rclativcl>. easy to synthcsizc. and ?;nowdon sr I’c&1

(1978) designed a study to test whether pygmy marmosets would distinguish bt’t~.ccn (II<.

two types of trills and whcthcr the trills arc responded to catcgoricatt~ or continuc~ust\..

Using a trill synthesizer, trills were created to vary in center frequency: frequency r-allgi,,

rate of modulation and duration. Since the Closed Mouth Trill and Open hlouth Trill L\ crc

identical except for duration, calls ofdiffercnt durations were synthesized, and the rcsponsc

frequency of pygmy marmosets was measured (as the presence or abst~nce ofan antiphonal

trill within 5s of the stimulus). Antiphonal responses to synthesized calls that mimicked the

range of natural Closed Mouth Trills were quite high. Responses to calls mimicking the

duration of average Open Mouth ‘I’rills were not difTerentiatty responded to than il‘ no

stimulus has been presented. Calls that were intermediate between the mean durations 01‘

the Closed Mouth and Open Mouth trills elicited a clear categorization. All trill duratiorls

between 176 to 249 ms were answered as if they were a normal Closed Mouth Trill. white

all trills of 257 ms or longer were answered as though no trill were present. OnI! a l’ew

milliseconds diKerence in duration at a critical boundary (e.g., 249 z’.r. 257 ms) produced

dramatically dillerent responses, while trills differing much more in duration (e.g., 176 ms

and 249 ms) were responded to as though they were identical (Figure 6). ‘Illus, py,qm)’

marmosets appeared to respond categorically to their calls ,just as human subjects do.

A similar study was done with the alarm call vocalizations of Goetdi’s monkey, C~ullimic~~

goeldi. Masataka (1983) had observed that wild Goeldi’s monkeys gave two types of

predator alarm calls. One elicited mobbing, and the other elicited freezing responses. Roth

calls appeared to be used discretely, but they could be placed on an acoustic continuum of.

frequency modulation. To determine how the monkeys perceived these calls LIasataka

synthesized the alarm trills, and presented captive animals with calls that wet-c lraried on

each acoustic dimension. He discovcrcd that frequency range was the most important

variable differentiating between the two \rocalizations. To calls varying in frequency range

between 1.6 and 2.4 kHz, the animals responded with antiphonal calling that led to a

mobbing response. To calls identical in all respects except varying in frequency range from

2.6 and 5.6 kHz, the monkeys responded with freezing responses. Thus, Masataka

identified a critical category boundary between 2.4 and 2.6 kHz of frequency range. These

results nicely parallel the situation found in pygmy marmosets (Snowdon & Pota, 1978).

However, do these studies indicate that monkeys are incapable of making fine acoustic

distinctions? This seems unlikely. A consideration of the social aspects of calling presented

a new perspective on such categorical response patterns. As with long calls. contact ~~11s

are likely to contain information on individual identity. Responses are likely to be

contingent upon who is calling rather than being reflexive responses to a call. Snowdon &

Cleveland (1980) demonstrated that, in pygmy marmosets, individual differences in the

structure of Closed Mouth Trills and J-calls existed and that diff‘ercnt animals responded

differently to playbacks of individual trills. Some of the individual difrerences were in

duration, the same dimension that differentiated between Closed Mouth and Open Mouth

Trills. In the Snowdon & Pota (1978) study, animals were presented with synthesized trills

that represented the average values for the population of pygmy marmosets. LVhat would

happen if animals were presented- with trills of specific familiar individuals? LVould the>

then display a greater sensitivity to dif%erences in duration?

The calls of several individuals were recorded and the paramrters of trills wcrc

measured. From these it was possible to define a set of parameters that could be used to

synthesize the calls of specific individuals. Since the duration dimension is the critical one,

VOCAL COMMUNICATIOS IN SEk’ 11’0RI.11 MOWKEYS 625

trills were synthesized according to the individual values for center frequency, frequcnc) range, and rate of modulation, while calls were varied systematically in duration

(Snowdon, 1987). Instead of asking animals to indicate bvhcther or not they perceived an average Closed Mouth Trill, we devised a test which allowed the animals to tell us if the

call they heard came from a particular individual. Snowdon & CXevrland ( 1980) discovered that calls played back throu,+ a speaker located in that individual’s home c-age.

elicited antiphonal calling by the other animals. However, il‘that individual’s c-all \\.a~

pla).ed back through a speaker in another animal’s cage, antiphonal calling was ,greatl~~

reduced. Thus, animals seemed to have expectations about where the calls of difTerc*nc

individuals should be coming from.

The synthesized calls of individuals were played back an equal number of times from the

cage where that individual lived and from other cages in the room. Ten trials wcrc

presented, at six different durations, both from the familiar and the unfamiliar location.

The results showed the same type ofcategorization as was found earlier when the responses

to all stimuli were combined. However, when the rcsponscs to different individuals wet-c

examined separately, it was clear that animals were using different categorical boundaries

which reflected their prior experience with the calls of that individual. For example, to thcl

synthesized calls of an animal that had very short trills. the animals rcspondcd o\.(‘r ;I

relatively much narrower range ofdurations. In gtmcral, responses to the synthcsizrd trills

of familiar individuals reflected the typical range of duration found in that individual’x

spontaneous calls.

The type of stimulus presented and the way in which the testing is done, can product-

both categorical responses with a rigid boundary dividing calls or may indicate that

animals make subtle distinctions of duration within a category. ‘rhis latter result occurs il’

the monkeys arc asked to detect the calls of a familiar individual. This result implies that

categorical responding is not biologically fixed. as kvith a perceptual fcaturc detrctor. but

rather is flexible and dependent upon a knobvledge of the call structure of familiar animals

(Snowdon, 1987). No similar studies have been done with human subjects. It is possiblt.

that categorical perception will be less clear in human subjects when socially familiar

speakers arc used to produce stimuli.

‘I’here is a clear distinction between CYosrd Mouth and Open Mouth Trills, but ~~11)

should there be three trill variants that seem to be used in similar contexts3 One possible

reason for the apparent redundancy relates to the function of contact calls. Animals not

onl!. need to identify which individual is calling, but the)- nerd to know where that

individual is located. Thus, contact calls should also contain cues for sound localixations.

However. makin%g one’s location known may risk attractin,? predators. .A compromise

solution would involve the use of ventriloqual calls when one is close to other group

members and to add information to improve localization on]\. as one becomes mor(~

separated from one’s own group.

How might sound localization be accomplished as part of the pygmy marmoset trill

series? There arc several acoustic features that can be used to convev location. DiKrrc*nccs

in the time of arrival of a sound to the two rars can indicate the direction of the source:

differences in the intensity of sounds heard at the two ears due to shadowing by the head

can also be used for localization. Recently, Brown (1982) has shown that frequcnc?

modulation is used by primates for sound localization. M:ith macaques, Brown tbund that

adding only 400 Hz of frequency modulation to a signal reduced the error of sound

localization by half. Howelrer, in a three dimensional test, which would be appropriate filr

626 K. ‘I‘. SNO\\‘lX)X

arboreal monkeys like the pygmy marmoset. it \vas nccrssar) 10 add at Ira~t L’ kHz 01‘

frequency modulation in order to impro\.c sound localization. Following thcsc principles.

the three pygymy marmoset trills can be rank ordered according to their h!,pothcsizcd c.asc’

of localization. The Quiet Trill always has less than 2 kHz of frequency modulation. ia

quite soft, so that intensity cues would be masked, and should, thrrt~fbrc, he difficult to

localize. At the other extreme, the J-call has 5-6 kHz offrequency modulation, well abo\~~

the critical threshold for localization in three dimensions, and is composed of frequentl>.

interrupted notes which present multiple time ofarrival cues. It should be easv to localize,.

The Closed Mouth Trill is structurally intermediate between the other two. a’nd it should

have intermediate localizability.

The functional prediction that would be made from these considerations of’

psychophysics is that in their natural habitat, pygymy marmosets should use Quiet Trills

when they arc close to one another and cues in other modalitics to locate the caller. .\s

animals get further and further apart there should he an increased usage of Closed Mouth

Trills and J-calls, with J-calls being used at the greatest distances. In a field study of the

pygmy marmoset in the Peruvian Amazon, Snowdon & Hodun ( 1981) recorded on a three

dimensional map of the home range the location ofthe caller and the location of the nearest

animal that could be detected. The distances between caller and recipient were calculated

and compared with the structure of the contact call used. Quiet ‘I‘rills were used, in fi1c.t.

when animals were close together and were rarely heard between animals more than 5 tn

apart. J-calls were used at the greatest distances, and were the onlv IGrm of trill used ~~hrrl

the caller was more than 20 m from the next nearest animal. Lastl~~, as predicted, the

Closed Mouth Trills were used at intermediate distances. (M? = 184.1, df = 13, t’ <WOO1

Closed Mouth Trill US. J-Call; X2 = 888.8, df = 13, P <O.OOl, Quiet Trill Z’S. J-Call; S” =

108.5, df = 8, P <O.OOl Closed Mouth Trill ~1s. Quiet Trill; Figure 7). Thus, the variation in

trill structure appears to be advantageous by increasing the locatabilit): of the caller in

proportion to the distance between conspecifics.

Do pygmy marmoset contact calls appear in adult form at an early age? \t’r have made

systematic recordings throughout the first year oflife. Closed Mouth ‘I’rills appear as earl!.

as the third week of life, but they differ from adult trills in structure and in context of usage.

Infant trills are higher pitched, ofshorter duration and more irregular in their li)rm. By the

end ofthe seventh week pitch is within the adult range, and by the end ofthe tenth week the

duration is within adult range. However, irregularities in structure appear throughout the

first year of life. The calls also are rarely given in the adult context during earl)- months.

and the trills arc often found juxtaposed with calls used hy adults in totally different

situations. Thus a contact trill may be cmittcd following an agonistic scream or a threat

vocalization. Pygmy marmoset infants engage in long bouts of solo calling or “babbling”. In these

babbling bouts a wide \,ariety of calls appear. Some are idiosyncratic. some arc identifiable

as elements of the adult repertoire, but given in strange juxtaposition. It is possible that

such babbling serves as practice, enabling young marmosets to acquire the adult structure

of calls. In addition, new infants born into the colony stimulate a regression toward infant

vocalizations by the older siblings. These observations suggest that the acquisition of calls

in pygmy marmosets may be more flexible than it appears to be in other primates.

Contact and af$liatirle calls of squirrel monke_vs Two forms of afilliative and contact calls in squirrel monkqys (Saimiri sciureus) have been

the subject ofextensive investigation, the isolation peeps and the chuck calls. The isolation

VOCAL C:OMMITNIC;ATION IN NEW W0RI.D MONliEYS 627

peeps of squirrel monkeys are brief, frequency modulated calls given by infants and

juveniles when separated from their mothers. There are two distinct morphs of squirrel

monkeys (which have been named after the circumorbital facial hair pattern) -the Roman

Arch animals generally found in the south and west of the Amazon River basin and the

Gothic Arch animals generally found in the north and east of the Amazon hasin

(Hershkovitz, 1984). Winter (1969) demonstrated that Roman Arch and Gothic Arch

infants produced distinctly different forms of isolation peeps, and Symmes rt al. (1979)

demonstrated through the use of discriminant analyses that the population or dialect

differences could be detected with success rates of 85-88s. Are these difrerences in

structure functionally important as well? Snowdon et al. (1985) tested groups of Roman

Arch and Gothic Arch squirrel monkeys with playbacks of \rocalizations of isolated.

unrelated infants from each of the two populations. The results were striking. 7’he Roman

Arch adult monkeys responded to the playback of Roman Arch infant isolation peeps I,!-

sho\ving increased locomotion, decreased huddling, and increased approach to the speaker

(Figure 8). In response to playbacks from Gothic Arch infants, however, there was no

change in behavior. The Gothic Arch adults behaved in just the opposite fashion. The!

responded with increased locomotion, decreased huddling, and increased approach onlv to

the c,alls of Gothic Arch infants. They ignored the calls of the Roman Arch infants. ‘I’hus.

the taxonomic significance of call structure is associated with identification cues that

apparently maintain the segregation of the infants according to population.

S>,mmes et al. (1979) also demonstrated that inc!i\idual differences could be discrrnccl

within each of the two dialect populations. This involved call parameters other than those

which signify population differences. These individual dift‘errnces were highly stable and

could be detected in samples of isolation peeps recorded during the first two years of lifi~

(Lieblich el al., 1980). Prior to the statistical determination of individual diflerenccs in

squirrel monkey isolation peeps, Symmes & Newman (1974) had shown via a conditioning

paradigm that squirrel monkeys could be trained to differentiate between variant forms of

the isolation peep, suggesting the capacity for individual recognition. Recentt)., Symmrs &

Hiben ( 1985) have demonstrated that the individual specific parameters of the isolation

prep can be used by mothers to recognize and respond to their infants. Mothers showed

sianilicantly greater responses to the playback sounds of their own infimts than to the,

sounds of other infants.

Masataka B Symmes (1986) systematically varied the distance between separated

intimts and members of their natal group. As distance increased, both infants and adults

cmplo\-tzd calls of increasing duration. They prolonged the high frequt‘ncy components 01

the call, which would make use of the ambient noise frequency window noted b)- Snowdon

& Hodun (1981 ). as welt as the high frequency attenuation that could serve to estimate

distance. Thus squirrel monkeys, like pygmy marmosets, appear to adjust their call

5tructurc according to how far they perceive themselves to be from other group mcmhers.

T’he role of learning in the ontogeny of vocalizations in squirrel monke),s has been th&

subject of considerable attention. Lieblich et a/. (1980) reported that individual and

])op~~lation-sp~~cilic characteristics of squirrel monke) vocalizations were essentialI)

unchanged from the first day of life through the second year, and Symmes et a/. ( I !)i!)) showed that tht. structure remained essentially unchanged through adulthood. Studies 01

tleal@ntd squirrel monkeys (Winter ef al., 1973; Talmage-Riggs rt al., 1972) Ibund I&

changes in vocal structure. Herzog & Hopl‘ (1984) reared squirrel monke1.s in social

isolation and when these monkeys were lirst presented M.ith the alarm call used to\Lxrd

628 c;. ‘I‘. SKO\Vl)O.\

avian predators, they ran to their mother surrogate. Alarm signals denoting terrestrial

predators also elicited retreat to the mother surrogate if the call was prcscntccl in

conjunction with a novel reference object. ‘I‘ogethcr thcsc studies suggest that early

auditory experience and early social interactions arc of’ little importance in the

development of vocal communication in squirrel monkeys. One might expect that calls

serving to reunite separated infants with their mothers, as well as alarm calls, might hc

quite conservative and less susceptible to early ontogenetic influences than other calls.

Newman Sr Symmes (1982) have examined the heritability of isolation peeps in hybrid

(Roman Arch X Gothic Arch) squirrel monkeys. Hybrids consistently inherit the maternal

facial pattern and isolation peep structures when their mothers arc of the Roman Arch

population. Among the hybrids, 98% of the isolation peeps recorded were of the Roman

Arch type suggesting that facial appearance and call structure are codominant. The close

parallel between maternal facial features and isolation peep structures was not as clear in

hybrids whose mothers were of the Gothic Arch population. Only 46% of their isolation

peeps were classified as the Gothic Arch type.

Two forms of affiliative vocalizations used between adult squirrel monkeys have been

described and analyzed by Smith et al. (1982a.6). The “chuck” call is specifically used by

Guv Per Bol Guv Per 601

Respondents Guyonese Per and Bol

Figure 8. Approaches to speaker by squirrel monkeys respondents (Guyanese or combined Bolivian and Peruvian) to playback of different infant isolation call stimuli (Guyancse. Peruvian or Bolivian) (from Snowdon et al., 1985).

VOCAL COMMI!NICATION IN NEW WORLD MOh-KEYS 629

t‘emales who have a close mutual social relationship. Females who interact with each other

in a close affIiative social relationship arc more likely to exchange chuck calls than arc

females which lack a close affiliative bond. Smith e/ al. consider this call to be a

mctacommunicative signal, communicating about the nature ofa social relationship rather

than an internal motivational state. Subscqurnt studies ha\,c indicated that there arc also

distinctive individual features within the chuck vocalization (Smith et al., 1982h) that can

l)e used retrospectively to identify individual females. Newman ~1 al. (1983) argued that

certain distinctive features of chuck call structure (a variable frequency modulated

component, a rapidly descending note and a terminal noisy element) are components that

also appear in the affllitative calls of other New \V’orld primates.

one additional afflliative call, the “err”, has been studied by Smith et a/. (1983). This is

given by females and it increases in frequency during the breeding season. ‘l‘he “err” is

associated with increased following and afflliative behavior by males. Thus it might be ;I

part of the squirrel monkey repertoire esclusive to the breeding season.

Complex .structures: grammar, dialogues and conversations

Among nonhuman primates the best examples of structurally complex vocalizations come

from New World primates. These involve both the complex structure ofvocalizations ,givcn

by an individual and the organization of calling betwren or among animals.

Robinson (1979) described the complex structural organization ofvocal sequences in the

titi monkey (Cal&bus moloch), which was fbund to repeat calls to form phrases and to

organize phrases into sequences. Six different sequence types were used in different

contexts. Playback stimuli were constructed with both the normal and abnormal phrase

sequences. Wht=n these stimuli were played back, titi monkeys responded differentlv to

each form, indicating that the animals perceived not only the individual components ofthc

sequences, but were also sensitive to their structural arrangement (or grammar).

In a study of capuchin monkeys (&bus oliuaceus), Robinson (1984) also found syntactic

orLganization of calls. Several identifiable syllables were used individually, but the). were

also combined to create compound calls. Fully 38% of the vocalizations analyzed b)

Robinson consisted of compound calls. The social contexts in which the compound calls

occurred were intermediate to the situations in which each of the units would have been

used alone, suggesting that the call combinations conveyed multiple internal states. This is

analogous to the unique word combinations used by human beings to express a synthetic

concept. These results indicate that some vocalizations of capuchin monkeys arc based on

lexical syntax. Marler (1977) described two types of syntax that might exist in animal

communication systems. The first, a phonological syntax, is analogous to the creation of

words with new meanings by combining or rearranging phonemes. The second form, a

lexical syntax, is the multiplexing of words with different meanings to represent a

combination of both. This type of syntax, Marler hypothesized, would be rare in animals.

A large proportion of the cotton-top tamarin repertoire consists of call segments that are

combined into phrases (Cleveland & Snowdon, 1982). rhllowing a series of simple

structural rules that appeared to be invariant. Most of these sequences are either

repetitions of calls which serve to intensify the effect of a single call, or combinations that

appear to be exatnples of “phonological syntax” where the meaning of a sequence dilt&-s

from the meaning of the component parts. However. <:le\,eland and Snowdon found IWO

630 K. .I‘.

cases described C’ebuJ 1,). Robinson ( 1984 I ( ht. combined an alarm call and a contact call, and was used in situations inhere the animals

were beginning to relax and move about after an alarm context. ‘l’he second c~ombincrl

territorial call, the F-chirp, which is given primarily by males in Lerritorial encounters. and

the Normal Long Call, which is given primarily by females (see McC:onnell 81 Snowdon.

1986). The combined call was given equally b)- both males and females at the peak 01

arousal during simulated territorial encounters. Newman et al. (1978) have also descrihcd rules which determine the sequencing 01

syllables within the twitter vocalizations of squirrel monkeys. DiA‘crent individuals used

different combinations of syllables, and different combinations were associated with

differential social contexts. In the pygmy marmoset, Pola & Snowdon (1975) described an

alarm call that appeared identical to a single syllable of the J-call contact vocalization.

Thus, the rate of repetition or number of notes may also be used to indicate context. ‘I‘hc

finding of syntactic rules governing the sequencing of calls, as well as the existence of lexical

syntax across so many New World primates species indicates the potential they 1laL.c for

complex communication.

Complex rules are also evident in the regulation of calling between animals. Ducts or

dialogues have been described in howler monkeys (Sekulic 1982a,6), titi monkeys

{Robinson, 1979; Kinzey & Robinson, 1983) and squirrel monkeys (Maurus et nl., 1985).

These interactions which involve regular patterns of calling in two animals, imply a close

coordination ofcommunication. Snowdon & Cleveland (1984) even found “conversations”

in pygmy marmosets. They observed a captive group of three monkeys and recorded the

sequences in which contact calls were given. Calls were not given randomly, rather there

was clear evidence of turn-taking. It was much more likely to find each animal calling once

before any individual called a second time. One particular permutation of “turns” was

significantly more likely to occur than the other possible combination. ‘l’hus, there

appeared tb be conversational rules for these vocal interactions. These rules might bt

adaptive in the wild, since each individual would call and be identilied in sequence. If an

animal failed to call in turn, other group members could respond appropriately.

When McConnell & Snowdon (1986) simulated territorial encounters in captive

cotton-top tamarins, there was a clear pattern of increased intensit). or escalation of calling over the course of the encounter. There were definite patterns of transitions between call

types both within groups and between groups. In general, escalations of aggrcssi\pc calls

came from animals in the same group where the previous call had originated. Animals in

the other group responded to the focal group with the same call they had previously heard.

Thus, here again, there appears to be some rules regulating the vocal cxchan,qes that occur

within and between groups during territorial encounters.

Summary

There evidence of complexity in vocal communication New World

Most New primates studied complex, highly vocal

repertoires. variations in are used subtly different situations. Playhack

indicate that monkeys themselves and respond to

these distinctions.

Pygmy show categorical of their just as

beings show perception of sounds but, with human the social

VOCAL COMMUNICATION IN NEW WORLD MONKEYS 631

context of communicating is important and animals can detect and respond appropriatel)

to dialect differences and to individual differences in call structure. While there is no

evidence that learning or experience is important in the ontogeny of squirrel monkey-

isolation peeps and alarm calls, studies on the long calls and contact calls in callitrichids

indicates some possible role for early esperience. Adult long call vocalizations develop

coincidentally with the attainment of sexual maturity, but they are preceded by a

“practice” phase of highly variable long calling similar to the plastic song phases found in

songbirds. Infant marmoset and tamarins show extensive “babbling”, and call structures

vary in predictable and reversible ways during development, suggesting the involvement 01‘

earl). learning. Finally, there is evidence of syntax. The existence of lexical syntax, and the

rule systems that seem to govern duetting, contact calling, and complex vocal exchanges

during territorial encounters are all found among the New World primates. No longer

should anyone be permitted to consider the New M’orld primates as “primitive”. espcciall)

with respect to their complex c0mmunicatL.e abilities.

Acknowledgements

The research reported here was supported by USPHS grants MH 29,775 and MH 35,2 I5 and a Research Scientist Development Award from the National Institute of Mental

Health. I thank the two reviewers for their critical comments on earlier versions of this

paper.

References

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M. R. Petersen, Eds) Primate Communication, pp. 144-l 70. New York: Cambridge University Press.

(:lrvcland,J. & Snowdon. C. T. (1982). The complex vocal rcpertoirc of‘thr adult cotton-top tamarin (.Y~,<u~w.Y

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