brotherhoods atelines

8/11/2019 Brotherhoods Atelines

1/17

BROTHERHOODS AMONG ATELINS:KINSHIP,AFFILIATION, AND COMPETITION

by

KAREN B. STRIER1)(Department of Anthropology, University of Wisconsin-Madison, Madison, WI 53706,

U.S.A.)

(With 3 Figures)

(Acc. 20-VII-1994)

Summary

This paper examines differences in male affiliative associations and dominance relation-ships in atelin primates. Despite the occurrence of male philopatry in all three genera, malesocial relations varied considerably. The strength of male affiliations was attributed todifferences in between group competition for access to groups of females, while the type ofmale dominance relationships was attributed to differences in within group competition foraccess to individual females. Female grouping patterns and the socionomic sex ratio

appeared to be more important than group size in predicting the strength of between groupcompetition and male affiliations. Male dominance over females appeared to be moreimportant than estrus synchrony in predicting the type of within group competition and thepresence of hierarchical or egalitarian relationships among males.

Introduction

Affiliative relationships among same-sexed primates have long been asso-

ciated with kinship and kin selection theory (HAMILTON, 1964). Because

extended matrilinies characterize the societies of many of the best-studied

1) A version of this paper was presented at the XIVth Congress of the InternationalPrimatological Society. I thank Dr. David HILLand Dr. Jan VANHOOFFfor inviting me toparticipate in their symposium, and for their valuable comments on earlier drafts of thismanuscript. Long-term field research on Brachyteleswas possible thanks to permission fromthe Brazilian government and CNPq, sponsorship by Dr. Celio VALLEand Dr. Gustavo DEFONSECA,and funds from NSF grants BNS-8305322, BNS-8619442, and BNS/DBS-8958298, theFulbright Foundation, grant no. 213 from the Joseph Henry Fund ofNAS,

the L.S.B. Leakey Foundation, WWF, the Graduate School of the University of Wisconsin-Madison, the National Geographic Society, the Chicago Zoological Society, and the LizClaiborne and Art Ortenberg Foundation. F. MENDES,J.RMOLl,A. RMOLl,P. COUTINHO,F.NERI,C. NOGUEIRA,L. OLIVEIRA,and A. CARVALHOcontributed to the long-term demo-graphic data described here.


2/17

152

Fig. 1.Dispersal patterns in anthropoid primates. Genera are added to each taxonomic groupin a cumulative way, such that the percentage plotted for cercopithecinesincludes fivegenera(listed below the x-axis), that plotted for colobines includes four colobine genera plus theoriginal five cercopithecine genera, and so on. Sources from Moore (1984, 1992);Pusey &

Packer (1987);Strier (1990).

primates, studies of affiliative relationships have tended to focus on

females (e.g. GouzouLES & GouzouLES, 1987). However, a growing bodyof data on a number of other species indicate that female philopatry and

male-biased dispersal are not as widespread among anthropoids as was

previously thought (MOORE, 1984, 1992). Indeed, female philopatry

appears to be a pattern only among the cercopithecine monkeys; when

other taxonomic groups are considered, dispersal and residency are evi-

dently quite variable (Fig. 1). Dispersal by both sexes occurs in manycolobines and apes, while female-biased dispersal coupled with male

philopatry are prevalent among the polygamous New World monkeys.The three genera that comprise the Atelin subfamily, Lagothrix, Ateles,

and Brachyteles, are particularly interesting subjects for examining affilia-


3/17

153

tive relationships among males: each lives in variably sized, extended

patrilineal groups resulting from female-biased dispersal and male phi-

lopatry (ROSENBERGER & STRIER, 1989; NISHIMURA, 1990a). Yet, the

nature of relationships among males differs strikingly in these closely-related genera. Evaluating the correlates of male affiliations and relation-

ships in the atelins may therefore provide useful insights into the bases of

male social behavior in other nonfemale-bonded primates.

A model for affiliations among male kin

Two parameters, or indices, of relationships among male kin can bereadily compared between taxa and studies. The first is the strength of

male affiliative associations, which can be assessed based on spatial

relationships, such as proximity and nearest neighbor preferences, and on

the frequency of affiliative interactions, including grooming partner and

embrace partner preferences (see FURUICHI & IHOBE, this volume, for

other examples). The second parameter is the type of relationships among

males, which can be characterized as hierarchical, based on agonistically-

determined dominance relations, or egalitarian, if agonistic competition

among males is rare or absent altogether (VAN SCHAIK, 1989).

1. Affiliative associations.

Variation in the strength of affiliative associations and in the type of

relationships among same-sexed primates has been attributed to variation

in the relative

importance

of betweengroup competition

and within

group competition, respectively (e.g. VANSCHAIK, 1989; VAN HOOFF & VAN

SCHAIK, 1992). Between group competition may lead to strong affiliative

associations that facilitate cooperation among males if such cooperationincreases males' access to groups of females. Whether such cooperation is

beneficial to males depends on behavioral and demographic variables

(HILL, this volume; VANHOOFF & VANSCHAIK, this volume). VAN HOOFF &

VAN SCHAIK (1992) postulate that fluid female grouping patterns and large

group size may make groups of females difficult for males to monopolizewithout cooperative efforts. In extreme cases, male cooperation in

between group competition may even be effective in herding females into

cohesive groups (WRANGHAM, 1980; see below). High socionomic sex


4/17

154

ratios, or the ratio of reproductive-aged females to males, might also

make it difficult for males to keep track of females, particularly among

large groupsof arboreal

primateswhere members

are frequently out ofvisual contact despite cohesive and coordinated movements. The socio-

nomic sex ratio may thus be an additional influence on male affiliative

associations and the benefits of cooperation in between group

competition.

2. Male relationships.

Strong male affiliations and cooperation in monopolizing groups offemales do not necessarily lead to tolerant, egalitarian relationships

among males within groups (VEHRENCAMP, 1983). Rather, male relation-

ships are expected to be hierarchical when within group competition is of

the contest type, such that males benefit by competing for access to

individual females. Egalitarian relationships among males, by contrast,should only occur when within group competition is of the scramble type,and aggressive competition among males does not improve their access to

individual females (VAN HOOFF & VAN SCHAIK, 1992). Thus, while maleaffiliative associations should reflect the degree to which groups of

females can be monopolized in between group competition, male domi-

nance relationships should reflect the degree to which individual females

can be monopolized by individual males in within group competition.There are at least two factors that determine whether contest competi-

tion among males increases a male's access to females. First, if female

estrus isasynchronous,

a dominant malemay

be able tomonopolizesexually-receptive females either directly, by preventing other males from

copulating, or indirectly, by restricting female choice (NEWTON, 1988;COWLISHAW & DUNBAR, 1991; VAN HOOFF & VAN SCHAIK, 1992). How-

ever, a male's ability to monopolize a female is also dependent on

whether males are individually dominant over females, and thus, on the

degree to which female mate choice can be expressed. If females are

dominant over, or codominant with, males, as in lemurs (YOUNG et al.,

1990) and Saimiri (BOINSKI, 1987), female choice may override maleefforts to monopolize copulations, and there may be few advantages to

overt competition among males (STRIER, 1990, 1992a). In this case,

egalitarian, rather than hierarchical, relationships should occur.


5/17


6/17

156


7/17

157

TABLE 1. Distribution of copulations across individual male Brachyteles.

Initials represent all adult and adolescent males in the group during each period, includingmales which were born and subsequently matured in the group. Numbers in parenthesesindicate the proportion of copulations by each male observed during the respective studyperiods. Only copulations in which the male participant was positively identified areincluded here. a STRIER,1987. b MENDES,1 990.present study, which includes continuousdata from March 1990-November 1992. d Disappearance and presumed death prior tosubsequent study period (see STRIER,1991, 1992c). " Adolescent male in 1983-1984, butfully adult by 1986-1987.

Agonistic interactions among group members were extremely rare, and

there was no evidence of any dominance hierarchy based on aggression,either among males, among females, or between males and females

(STRIER, 1986, 1990, 1992a,c). Yet, despite the absence of overt competi-

tion, there were pronounced differences in male mating success (Table 1).These differences were evident across males during the same period, and

for particular males across successive years. For example, the most sexu-

ally-active male between 1983-1984 and 1986-1987, IV, accounted for38.5% and 50.0% of observed copulations, respectively. By the

1990-1992 period he accounted for only 15.4% of observed copulationswhile a younger male, DA, born in 1985, accounted for 20.4%. DA is the

only sexually-active male positively known to have an older maternal

brother, DI, in the group, and it is tempting to infer that DI aided his

younger brother in securing mates. However, we found no evidence for

coalitions between these males.

Copulations routinely occurred in full view of other group members(STRIER, 1992c), and nearly all adult and subadult males were observed to

copulate across the three study periods analyzed here (Table 2). The

proportion of copulating males approached 100% as both the number of


8/17

158

TABLE 2. Changes in the distribution of group male versus extra-group

male copulations

All data refer to study group males except "% males identified", which includes both studygroup and extra-group males, and "% copulations by ja6 malcs", or males from aneighboring group and thus, extra-group males. Sources as in Table 1.

observed copulations and the number of males which could be positivelyidentified during these copulations increased. Although we currently lack

information on paternity, and therefore male reproductive success, it was

evident that males did not compete aggressively to monopolize estrous

females. The fact that the distribution of copulations was nonethelessstrongly skewed across males suggests that female mate choice may be

responsible for differential mating success among male Brachyteles.Females demonstrated their ability to assert mate choice by actively

initiating sexual inspections and copulations with particular males, and

by avoiding unwanted attention from others by simply walking away

(STRIER, 1992a, c). Some females exhibited strong preferences for particu-lar males, but it is not evident what male attributes these preferences were

based on (STRIER, 1992a, in prep.). Copulations tended to be seasonal

(STRIER, 1991), but females did not exhibit tight estrous synchrony.

Rather, the inability of males to dominate females appeared to be respon-sible for the high degree of tolerance males exhibited toward one

another's mating activities, and for the apparent nonaggressive relation-

ships among them (STRIER, in press).While male Brachyteles did not compete overtly with other males in their

group for sexual access to females (STRIER, 1992a), relationships betweenmales from different groups were hostile. Male group members joinedforces in prolonged vocal displays and chases when males from a neigh-

boring group at this site were encountered, and often they succeeded in


9/17

159

leading their female associates away from male intruders (STRIER, 1986,

1992c). As group size, female subgrouping, and sex ratio increased,

however, even such cooperative efforts became increasingly less effective.During the first six years that these Brachyteles were observed, the adult

females in the group remained together as a cohesive unit (STRIER, 1991)and the six adult males were successful at preventing incursions by extra-

group males. Since 1988, however, males from a neighboring group, Jao,

began to account for a substantial proportion of copulations with groupfemales (Table 2).

Demographic changes in the group may have been responsible, at least

in part, for what appeared to be a decline in male between group

competitive ability (Table 2). Between 1982 and 1992, the study groupmore than doubled in size, increasing from its original 22 members to 48

members. The socionomic sex ratio also jumped dramatically, increasingfrom 1.1 in 1987 to 1.7 in 1988 due to the presumed deaths of two adult

males and the documented maturation of adolescent females which had

previously immigrated. This increase in sex ratio coincided with a

number of otherchanges

in thegroup, including

agreater tendency by

group females to fission into smaller temporary feeding parties (STRIER et

al., 1993), as well as a greater proportion of copulations by extra-groupmales (Table 2).

2. Ateles.

Descriptions of affiliative associations among male Ateles appear to be

comparable to those among male Brachyteles. A. geoffroyl, studied at Tikal,Guatamela, exhibited significantly higher rates of affinitive interactions,

including sitting in contact, embracing, touching, and grooming, than did

females, and males directed 85% of all affinitive interactions toward other

males (FEDIGAN & BAXTER, 1984). At Manu National Park, Peru, associa-

tion indices for A. paniscus males were more than twice as high, on

average, as those of females. These males also groomed one another

significantly more than

expectedby their representation in the study

population (SYMINGTON, 1987, 1990).

Despite their strong affiliations, however, Ateles male relationships

appeared to be hierarchical rather than egalitarian, even among male

subgroups. SYMINGTON(1987) observed that although all males were likely


10/17

160

TABLE 3. Correlates of male associations

Data for Lagothrix(5 studies)and Ateles(5 studies)are summarized from NISHIMURA'S(1990a)review; data from Brachytelesare based on the present study of a single group over a 10 yearperiod. BGC, or between group competition, is discussed in the text. Categorical designa-tions are based on cited literature.

to have copulated during her 12-month study, the dominant male was the

only male which mated in view of other group members instead of in

seclusion. Ateles males are dominant over females, and relationshipsbetween the sexes are reportedly tense (FEDIGAN & BAXTER, 1984; SYM-

INGTON, 1987).Affiliative associations among male Ateles have been attributed to the

importanceof male coalitions

during intergroupencounters

(WRANGHAM,1980; SYMINGTON, 1987, 1990). Not only are female grouping patterns in

Ateles fluid, the socionomic sex ratio of nearly all groups studied to date is

higher than that of other atelin groups (NISHIMURA, 1990a). Both of these

conditions are consistent with predictions that male cooperation is critical

in between group competition over access to a relatively large number of

dispersed females (Table 3).The advantages of cooperation in between group competition do not

appear, however, to override the advantages of within group contestcompetition in Ateles or in Pan, a species which exhibits remarkable

behavioral parallels with Ateles (SYMINGTON,1990; FURUICHI & IHOBE, this

volume). Like Brachyteles, Ateles females do not experience tightly syn-chronized estrus, but unlike Brachyteles, Ateles males are dominant over

females (Table 4). Male dominance in Ateles, but not in Brachyteles, may be

related to other differences between the genera. Both genera exhibit

relatively low levels of sexual dimorphism in body size, but canine dimor-

phism may be more pronounced in Ateles than in Brachyteles (ROSENBERGER& STRIER, 1989). Brachyteles, however, have extraordinarily large testes

size, suggesting that males may employ more subtle forms of sperm

competition (MILTON, 1985; STRIER, 1986, 1992a, c) than Ateles, which


11/17

161

TABLE 4. Correlates of male relationships

WGC, or within group competition, is discussed in the text. Categorical designations arebased on cited literature, summarized in NISHIMURA(1990a) and the present study.

have small testes and compete overtly (FEDIGAN & BAXTER, 1984). Fur-

thermore, male coalitions in chasing Ateles females (FEDIGAN & BAXTER,

1984; SYMINGTON,1987) have not been observed in Brachyteles, raising the

intriguing possibility that Ateles males achieve their dominance over

females through cooperative efforts.

3. Lagothrix.

Male affiliations inLagothrix appear

to be weaker thanthose

inthe otheratelins, but their hierarchical relationships resemble those of Ateles. Male

L. lagotricha, studied in the upper Colombian Amazon, were rarelyobserved in close proximity to one another (NISHIMURA, 1990a). Males

were proportionately more interactive with one another than were

females, due largely to higher frequencies of play among juvenile and

subadult males, and higher frequencies of agonistic interactions amongmales. NISHIMURA(1990a: 115) concludes that "... so far as only adults are

concerned, it could not be said that males are more associative (with) oneanother than females."

Dominance relationships among Lagothrix males were based on the

outcomes of agonistic interactions, and appeared to be related to age

(NISHIMURA,in prep.). At La Macarena, Colombia, male rank correlated

with the frequency of affiliative interactions with females, and the domi-

nant male mated more frequently (31.7%) than others. (NISHIMURA,

1990b). Nonetheless, every male accounted for at least 13.7% of observed

copulations, suggesting that the variance in male mating success was

lower in Lagothrix than in the more egalitarian Brachyteles.The absence of strong affiliative associations among Lagothrix males

appears to correspond to an absence of tension between groups.


12/17


13/17

163

Atelin comparisons indicate two possible additions to VAN HOOFF &

VAN SaHam's (1992) model. First, these comparisons suggest that group

size may not be as important as previously assumed in predicting cooper-ative affiliations among males in between group competition, at least in

primates which exhibit flexible grouping patterns. Intraspecific variation

in group size is similar across all atelins, with reported group sizes rangingfrom lows of 10 and 16 in Lagothrix and Ateles to highs of 45, 42, and 48 in

Lagothrix, Ateles, and Brachyteles, respectively (Table 3; NISHIMURA, 1990a).All Ateles groups studied to date have fluid grouping patterns regardless of

group size, but some Lagothrix groups are reportedly more fluid than those

considered here (see DEFLER, 1987; SOINI, 1987), and Brachyteles groups atother sites have been described as both fluid (MILTON, 1984) and cohesive

(LEMOS DE Spa, 1988). Data on male social relationships, sex ratios, and

intergroup encounters are needed from these other Lagothrix and Bra-

chyteles populations before further intraspecific comparisons can made.

Demographic changes in the Brachyteles group described here suggestthat increases in both group size and sex ratio were associated with

increasinglyfluid associations

among females, implyingthat lower levels

of within group feeding competition among females and/or male cooper-ative efforts were responsible for the cohesion that characterized this

group during the first six years of observation (STRIER et al., 1993). The

greater tendency toward fluid grouping patterns in this study group has

led to the proposition that Brachyteles groups are facultatively cohesive

(STRIER, 1989, 1992b), particularly when food patches are large enoughto support all group members (see also STRIER, 1986; LEMOS DE SA &

STRIER, 1992). While fluid grouping patterns were consistently associatedwith strong male affiliative relations in Brachyteles as well as in Ateles, it is

not clear whether increased group size (relative to food patch size) or sex

ratio is responsible for their fission-fusion social organization.

Second, the exceptional egalitarian relationships among Brachyteles

males, in contrast to the hierarchical relationships in Lagothrix and Ateles,

suggest that the ability of males to dominate females is an importantdeterminant of whether within group competition among males is of the

contest or the scramble type. Even when estrus is asynchronous, as is the

case in all three atelins, female codominance in Brachyteles may reduce the

advantages of contest competition among males, increase the oppor-tunities for female mate choice, and lead to egalitarian relationships that


14/17

164

Fig. 3. Factors contributing to male affiliative behavior in atelins.

facilitate, but are not necessary for, male cooperation in between group

competition.

Indeed, the atelins provide suggestive evidence that kinship, affiliative

associations, and cooperation among males in between and within groupcompetition do not always co-vary (Figure 3). Kinship need not lead to

strong affiliative associations or cooperation among male group members

when between group competition is low (VANHOOFF & VAN SCHAIK, this

volume), as appears to be the case in Lagothrix. Even when cooperation

among male kin in defending groups of females in intergroup encounters

occurs, as in Ateles and Brachyteles, contest competition among the same

males over access to individual females occurs in Ateles but not in Bra-

chyteles due to differences in the type of within group competition. More-over, male cooperative coalitions have been observed in other primateseven when there is little evidence of affiliative associations outside of

agonistic contexts (e.g. PACKER, 1979; SMUTS & WATANABE, 1990). Con-


15/17

165

versely, strong affiliative associations may occur between males which

nonetheless fail to support one another in agonistic interactions (HILL,

this volume).Further data on the correlates of within group competition are needed

from species in which dispersal and philopatry are not sex-biased, and in

which dominance relationships between males and females are more

equitable. Similarly, long-term demographic and behavioral data are

needed from a greater number of species in order to better understand the

interactive effects of sex ratios and male dominance on the dynamics of

male competition and social relationships between and within primate

groups.

References

BOINSKI,S. (1987). Mating patterns in squirrel monkeys (Saimirioerstedi)._ Behav. Ecol.Sociobiol. 21, p. 13-21.

COWLISHAW,G. & DUNBAR,R.I.M. (1991). Dominance rank and mating success in maleprimates. - An. Behav. 41, p. 1045-1056.

DEFLER,T.R. (1987). Ranging and the use of space in a group of woolly monkeys (Lagothrix

lagotricha)in the NW Amazon of Colombia. - Internat. J. Primatol. 8, p. 420.FEDIGAN,L.M. & BAXTER,M.J. (1984). Sex differences and social organization in free-

ranging spider monkeys (Atelesgeoffroyi).- Primates 25, p. 279-294.FURUICHI,T. & IHOBE,H. (this volume). Variation in male relationships in bonobos and

chimpanzees.GOUZOULES,S. & GOUZOULES,H. (1987). Kinship. - In: Primate societies. (B.B. SMUTS,

D.L. CHENEY,R.M. SEYFARTH,R.W. WRANGHAM& T.T. STRUHSAKER,eds). Univer-sity of Chicago Press, Chicago, p. 299-305.

HAMILTON,W.D. (1964). The genetical evolution of social behaviour. I and II. -J. theor.Biol 12, p. 1-52.

HILL,D.A. (this volume). Affiliative relations between adult males of the genus Macaca.

VANHOOFF,J.A.R.A.M. & VANSCHAIK,C.P. (1992). Cooperation in competition: theecology of primate bonds. - In: Coalitions and alliances in humans and otheranimals. (H.A. HARCOURT& F.B.M. DEWAAL,eds). Oxford University Press, Oxford,p. 357-389._ _ &_ _ (this volume). Male bonds: affiliative relationships among nonhuman primatemales.

LEMOSDES, R.M. (1988). Situao de uma populao de mono-carvoeiro, Brachytelesarachnoides,em fragmento de mata Atlntica (M.G.), e implicaotilde;espara sua conser-vao. - MA thesis, Universidade de Brasilia.

_ _ & STRIER,K.B. (1992). A preliminary comparison of forest structure and use by twoisolated groups of woolly spider monkeys, Brachytelesarachnoides.- Biotropica 24,

p.455-459.MENDES,F.D.C. (1990).Affilio e hierarquia no muriqui: o grupo Mato de Caratinga. -MA thesis, Universidade de So Paulo.

MILTON,K. (1984). Habitat, diet, and activity patterns of free-ranging woolly spidermonkeys (BrachytelesarachnoidesE. Geoffroy 1806). - Internat. J. Primatol. 5, p.491-514.


16/17

166

_ _ (1985). Mating patterns of woolly spider monkeys, Brachytelesarachnoides:implicationsfor female choice. - Behav. Ecol. Sociobiol. 17, p. 53-59.

MITCHELL,C. (this volume). Migration alliances and coalitions among adult male SouthAmerican

squirrel monkeys (Samirisciureus).MOORE,J. (1984). Female transfer in primates. - Internat. J. Primatol. 5, p. 537-589._ _ (1992). Dispersal, nepotism, and primate social behavior.

- Internat. J. Primatol. 13,p. 361-378.

NEWTON,P.N. (1988). The variable social organization of hanuman langurs (Presbytisentellus),infanticide, and the monopolization of females.

_ _Internat. J. Primatol. 9, p.59-77.

NISHIMURA,A. (1990a). A sociological and behavioral study of woolly monkeys, Lagothrixlagotricha,in the upper Amazon. - Sci. Eng. Rev. Doshisha Univ. 31, p. 87-121.

_ _ (1990b). Mating behavior of woolly monkeys (Lagothrixlagotricha)at La Macarena,Colombia (II): mating relationships.

- Field Studies of New World Monkeys, La

Macarena,Colombia

3, p.7-12.

PACKER,C. (1979). Male dominance and reproductive activity in Papio anubis. - An.Behav. 107, p. 37-45.

PUSEY,A.E. & PACKER,C. (1987). Dispersal and philopatry.- In: Primate societies. (B.B.

SMUTS,D.L. CHENEY,R.M. SEYFARTH,R.W. WRANGHAM& T.T. STRUHSAKER,eds).University of Chicago Press, Chicago, p. 250-266.

ROSENBERGER,A.L. & STRIER,K.B. (1989). Adaptive radiation of the ateline primates. -J.Hum. Evol. 18, p. 717-750.

VANSCHAIK,C.P. (1989). The ecology of social relationships amongst female primates.-

In : Comparative socioecology, the behavioural ecology of humans and other mam-mals. (V.S. STANTON& R.A. FOLEY,eds). Blackwell Scientific, Oxford, p. 195-218.

SMUTS,B.B. &

WATANABE, J.M.(1990).Social relationships and ritualized greetings in adult

male baboons (Papiocynocephalusanubis)._ Internat. J. Primatol. 11, p. 147-172.SOINI,P. (1987). Ecology of Lagothrixlagotrichaon the Rio Pacaya, northeastern Peru.

-

Internat. J. Primatol. 8, p.421.STRIER,K.B. (1986). The behavior and ecology of the woolly spider monkey, or muriqui

(BrachytelesarachnoidesE. Geoffroy 1806).- PhD thesis, Harvard University.

_ _ (1987). Reproduo de Brachytelesarachnoides.- In: A primatologia no Brasil- 2. (M.

THIAGO.DE.MELLO,ed.). Sociedade Brasileira de Primatologia, Brasilia, p. 163-175.

_ _ (1989). Effectsof patch size on feeding associations in muriquis (Brachytelesarachnoides).- Folia Primatol 52, p. 70-77.

_ _ (1990). New World primates, new frontiers: insights from the woolly spider monkey,or muriqui (Brachytelesarachnoides).- Internat. J. Primatol. 11, p. 7-19.

_ _ (1991). Demography and conservation of an endangered primate, Brachytelesarach-noides.- Conserv. Biol. 5, p. 214-218.

_ _ (1992a). Causes and consequences of nonaggression in the woolly spider monkey, or

muriqui (Brachytelesarachnoides).- In: Aggression and peacefulness in humans andother primates. (J. SILVERBERG& J.P. GRAY,eds) Oxford University Press, New York,p. 100-116.

_ _ (1992b). Atelinae adaptations: behavioral strategies and ecological constraints.-

Amer. J. phys. Anthrop. 88, p. 515-524._ _ (1992c). Faces in the forest: the endangered muriqui monkeys of Brazil. Oxford

University Press, New York._ _ (in press). Subtle cues of social relations in male muriqui monkeys (Brachytelesarach-

noides).- In: New world primates: evolution, ecology and behavior (W.G. KINZEY,ed.). Aldine de Gruyter, New York.

_ _, MENDES,F.D.C., RMOLI,J.&RMOLl,A.O. (1993). Demography and social structurein one group of muriquis (Brachytelesarachnoides).

- Internat. J. Primatol. 14, p.513-526.


17/17

167

SYMINGTON,M.M. (1987). Ecological and social correlates of party size in the black spidermonkey, Atelespaniscuschamek.- PhD thesis, Princeton University.

_ _ (1990). Fission-fusion social organization in Atelesand Pan. _ Internat. J. Primatol.

11, p. 47-61.VEHRENCAMP,S.L. (1983).A model for the evolution of despotic versus egalitarian societies._ Anim. Behav. 31, p. 667-682.

WRANGHAM,R.W. (1980). An ecological model of female-bonded primate groups. -Behaviour 75, p. 262-299.

YOUNG,A.L., RICHARD,A.F. & AIELLO,L.C. (1990). Female dominance and maternalinvestment in strepsirhine primates. - Am. Nat. 135, p. 473-488.

brotherhoods atelines

Documents