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Development and social dominance among group-living primates.

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American Jo u rn al of Primatology 37:143-175 (1995)
Development and Social Dominance Among
Group-Living Primates
MICHAEL E. PEREIRA
Duke University Primate Center, Durham, North Carolina
Organisms are integrated systems whose physical and behavioral components codevelop and coevolve. Ontogenetic requirements in one domain
are satisfied in part by prior or concurrent developments in another. This
work explores how characteristic growth patterns in two primate groups
interact with ecological, social, and other life-history constraints to promote the development of particular systems of agonistic relationship.
First, the markedly size-dimorphic savanna baboons are contrasted with
relatively nondimorphic macaques, where the pubertal growth capacity of
males, relative to that of females, is comparatively modest. In baboons and
other dimorphic Papionines, maturing males can be expected to invest
more heavily in successful feeding competition, and known variation in
the ontogeny of male-female dominance relations is well explained by this
prediction. Data from five of the best-known species, for example, suggest
that the female inclination to promote offspring dominance over male
peers before puberty diminishes with increases in relative male size and
growth potential a t puberty. Potential mechanisms for the development of
this pattern are discussed. Next, ontogenies are considered for ringtailed
lemurs, a highly social, monomorphic prosimian primate in which seasonal scheduling of growth causes a large proportion of adult size to be
achieved before weaning. In this species, daughters invariably develop
strong alliances with their mothers, and pubertal females must overturn
adults in dominance to remain in large natal groups. Despite life-history
parallels between ringtails and the focal Papionines, the lemurs do not
collaborate agonistically in ways that ensure matrilineal “inheritance” of
dominance status, as seen in the monkeys. Body weight and individual
fighting ability appear to determine dominance relations among infants,
and asymmetries established before weaning typically remain stable until
sexual maturation. Anatomical and behavioral data suggest that low visual acuity prevents ringtailed lemurs from developing a system of agonistic intervention that could stabilize adult dominance hierarchies and
mediate rank inheritance. In any case, failure to promote the dominance of
close kin is argued to have influenced life-history evolution in ringtailed
lemurs extensively, including aspects of growth, reproductive biology, and
social structure. These analyses identify foci for future research and illus-
Received for publication May 5, 1993; revision accepted September 19, 1994
Address reprint requests to Michael E. Pereira, Dept. of Biology, Bucknell University, Lewisburg,
PA 17837.
0 1995 Wiley-Liss, Inc.
144 I Pereira
trate the importance of bidirectional effects and feedback in the development and evolution of primate life histories and behavior.
0 1995 Wiley-Liss, Inc.
Key words: primates, life history, development, growth, social dominance,
social systems
INTRODUCTION DEVELOPMENT AND BEHAVIOR
If [we] were concerned only with the unsolved problems of biology, 90 per cent
of [our attention] would be devoted to two topics: behaviour and development. In
these fields, we are not even certain what kind of solution we are seeking. [Smith,
19861
The organism is a n integrated whole, genotype with phenotype . . . in t u r n part
of a nexus of ecological and sociocultural relationships which extends from the past
and into future generations. Development and evolution are therefore intimately
connected. . . not separate as conceived within Neo-Darwinism. [Ho & Fox, 19881
There is no holding nature still and looking a t it [Whitehead, 19201.
Life is a complicated phenomenon [sensu Salthe, 19851, and principals of development and behavior remain elusive. Individual organisms are integrated systems whose components comprise anatomy and physiology, including the hormonal and neurologic subsystems that exist in some species to help structure and
guide behavior. Expression of the genome inherited a t conception firmly directs
initial aspects of development, and some genetic variability among individuals is
ultimately reflected in divergent life histories. Male vs. female ontogeny in any
sexually reproducing species offers one compelling example. Natural selection can
also foster genetic variability, or differential genetic expression, among members
of one sex or populations of a species, when divergent life-history “strategies”
maximize reproductive potential for different sets of individuals in particular environments [e.g., Etter 1989; Crow1 & Covich, 1990; Reznick et al., 1990; Shuster
& Wade, 19911.
Nevertheless, individual genes code only for proteins. Distinctive cell or tissue
types are not represented a s such in the genetic code, let alone such things as fully
developed pituitary glands or gonads or the developmental and behavioral processes influenced by their interaction. All such high-order phenotypic characters
are the products of development: the inter-nested, self-organizing processes of organismic change and integration that occur, a t every level, across the life spans of
individuals, groups, populations, and communities [Oyama, 1985; Ho, 19881. The
very essence of development is responsiveness to the environment, and both environment and response can include influences of and on genetic expression. Understanding organismic development is paramount to progress in virtually every biological subdiscipline, and considerable work in many-including
genetical
ecology, systematics, and life-history theory-is devoted to the goal [e.g., Schlichting & Levin, 1986; Stearns & Koella, 1986; van Noordwijk et al., 1988; Reznick,
1990; Salthe, 1993; Hall, 19941.
Across a n animal’s life span, its behavior mediates between its physiology and
its environment in the broadest sense. Thus, behavior can be expected to play
crucial roles in development. Animals modulate behavior to thermoregulate, to
respond to caretakers, to disperse and identify conspecifics, to find and compete for
resources, to avoid predators, and to care for offspring. Much behavior in each of
these categories is heavily canalized: just as traditional taxonomy describes degrees of physical resemblance among classes of animal, so too behavioral repertoires have repeatedly been shown to distinguish phyletic groups [e.g., Struh-
Development an d Dominance Among Primates I 145
saker, 1970; Huntingford & Turner, 1987; Macedonia & Stanger, in press; Pereira
& Kappeler, in press]. This should not surprise, given that behavioral subsystems,
within and between individuals, coevolve with associated physical subsystems.
Ontogenetic requirements in each domain are met in part by prior and concurrent
developments in the other. Examples to recall are many: bone and muscle must
interact for either to develop normally [Gray, 19771; mammals denied patterned
visual input early in life fail to maintain the neuroanatomy necessary to discriminate shapes visually [Thompson, 19751; and Hines [1942] showed long ago how the
intimate mother-infant relationship in primates depends initially on antecedent
neurological developments underlying the infantile grasp reflex.
Development and behavior, then, are crucial and reciprocally dependent elements of animal life histories, and, as life-history theory has developed, investigators of behavioral ecology in primates and other mammals have used it increasingly as a framework for their research [e.g., Altmann, 1980; Rubenstein, 1986;
Bekoff et al., 1987; van Noordwijk et al., 19931. Because evolution is, a t its essence,
the ecological control of development, and because no single-life-history feature
better distinguishes primates among mammals than protracted development
[Pereira & Fairbanks, 19931, a n important theoretical adjustment for upcoming
years of behavioral primatology will be to recognize mating systems research as
but one component of research on developmental systems. From this vantage,
biologists begin to ask how aspects of physical and behavioral development interact and, a t another level, how developmental phenomena simultaneously structure
and respond to systems of social behavior.
These two questions lie at the heart of this paper, in which I provide overviews
of development of adult body size (somatic growth) and of social dominance in
separate primate groups and propose functional and specific causal relationships
between these ontogenetic domains. The primates comprise two of the very few
groups for which appreciably detailed information has become available on both
developmental processes. On the one hand, I interpret data on macaques (Mucaca
spp.) and savanna baboons (Papio cynocephalus subspp.), cercopithecid Anthropoids hereafter referred to as the Papionines (though few relevant data exist for
other members of this tribe). On the other, I discuss ringtailed lemurs (Lemuridae:
Lemur cuttu), a species behaviorally much unlike any other lemur and the most
gregarious primate in the prosimian suborder.
The work is neither a conventional review nor a traditional empirical report.
It is meant to contribute by helping to relate work on primate behavior, including
some on perception and cognition, more closely to the theoretical framework of
life-history analysis and to relate life-history analysis to concepts of behavioral
development. Readers should note a t this juncture that published information on
growth and on development of dominance for even our focal taxa is substantially
incomplete. No part of me, in presenting this work, means to imply that suggested
interpretations are unassailably supported by existing data. To the contrary, missing data preclude not only extension of my analysis to closely related taxa but even
satisfactory evaluation of ideas in relation to the focal species, undeniably among
the best-described of all primates. As such, many of my interpretations are solely
predictive or openly speculative. Most important, however, the two analyses together provide a basis from which the data most important to further evaluation of
these and competing ideas can readily be targeted during future research on primate life history, development, and behavior.
This paper does bring together information on some well-documented patterns
of development, patterns that have been analyzed only separately before but need
also to be cointerpreted. The analysis is facilitated by the fact that the focal groups
146 I Pereira
share basic commonalities in life history, including certain close similarities in
social behavior. Also, I have personally studied representatives of each ( M .fuscutu:
1977-1979; P. c. cynocephalus: 1980-1984; L . cattu: 1985-present [methods and
more complete results in Pereira, 1986, 1988a,b, 1989, 1993b,c; Pereira & Weiss,
1991; Pereira & Kappeler, in press]). It lies beyond my present objective to provide
any of the many missing data or to try to interpret all related phenomena (e.g.,
variation in papionine dimorphism). Rather, I seek to identify plausible relationships between characteristic patterns of growth and dominance development in
two dominance-oriented groups of primates. In concluding, I attempt to show how
primate social systems will only ever be fully understood through multifaceted
analysis of individual development in relation to all aspects of life history.
Primate Social Dominance, Development, and Assumptions
Many group-living primates reliably develop species-typical systems of agonistic interaction that are organized around social dominance. In a dominance
relationship, a subordinate individual employs a repertoire of submissive behavior
to circumvent and allay aggression by a dominant groupmate [Bernstein, 19813. In
species where dominance is frequently and unambiguously expressed-including
all featured in this work-dominants unequivocally use their status and aggression to garner access to resources (e.g., food, mates, shelter), even to the extent of
expropriating it from subordinates. While it is conceptually reasonable that one
individual might dominate another in conflicts over only certain types of resources
(e.g., food but not mates), this is not generally found to be true among nonhuman
primates with salient dominance behavior. Instead, dominants in these taxa use
their status and aggression in efforts to obtain all sorts of resources, whether or not
it seems sensible to researchers! Primates exhibiting such dominance behavior are
the only species to which all aspects of the present analysis could reasonably be
applied.
The first of three principal assumptions underlying this analysis is that dominance exists in our focal taxa because it can enhance for superiors access to
resources and mitigate for inferiors rates and effects of aggression received,
thereby promoting individual survival and reproductive success. These are not
new or radical ideas [Allee, 1938; Tinbergen, 19531. Neither do they ignore important bodies of recent research showing that (1)alternative tactics enable subordinates to access resources (e.g., alliance formation), (2) particular demographic and
ecological factors diminish the effectiveness of dominance (e.g., small, dispersed
food), (3)primates often withhold their dominance (e.g., versus kin or “friends”), (4)
different styles of dominance exist among even closely related taxa [Thierry, 1985;
de Waal, 19891, and ( 5 ) many primates seem not to do dominance a t all [e.g.,
Rowell, 1988; Watts, 1994; Pereira & Kappeler, in press]. These factors all reduce
the predictability of effects of agonistic asymmetries between primates and help
keep primate agonistic relations an important and complex domain of scientific
inquiry. None contradicts our first basic premise, however (see Harcourt 119871
and Silk [1993al on dominance and reproductive success and Barton and Whiten
[19931 on dominance and feeding competition).
Our remaining assumptions relate to the nature of development in primates.
Mammals are considered juvenile from the time that they could survive the death
of their caretaker until they mature sexually [Pereira, 1993al. From the viewpoint
of evolution, with the principal objective of reproduction, juvenility should not
exist a t all in a life history, whenever possible. Delay of maturation is often beneficial, however, in an animal’s effort to survive an interim harsh season or simply
to maximize the resources available to sponsor growth [Pereira, 1993al. That re-
Development and Dominance Among Primates / 147
sources must be allocated among maintenance, growth, and reproduction is a basic
prediction of life-history theory that has received widespread empirical support in
research on both plants and animals [Roff, 19921.
Many anthropoid primates present an unusual pattern, however, in that many
are moderately large but do not grow as fast as they are physiologically capable.
Formerly, this slow growth was presumed to function in relation to the time primates needed to learn all that they seemed to have to learn, including the complexities of their social behavior [e.g., Poirier, 1972; cf. Schulz, 19691. Reviewing
much recent research, Janson and van Schaik [19931 showed that, in fact, most
learning seems largely accomplished long before maturation in primates. Other
pivotal consequences of life in large social groups, they argued, are that immatures
are sheltered from predation risk while they experience immediate disadvantages
in feeding competition. Juvenile primates, the authors suggested, exploit the option of slow growth in their protected environment to safeguard themselves
against high instantaneous risk of death due to malnourishment.
Our second assumption, then, is that primates are inherently risk-averse
throughout most of prereproductive development [Janson & van Schaik, 19931. As
nonreproducers, juveniles can enhance their immediate fitness only by promoting
their chances of survival. While certain behavioral adjustments may augment
future fecundity, juvenile primates should favor survival over potentially improved futures whenever faced with conflicting options [e.g., van Noordwijk et al.,
19931. Whenever dominance acquisition entails particularly risky agonistic conflict for immatures, therefore, it would be reasonable to infer that probability of
survival is at stake.
Primates do not differ from most other determinate growers in that they postpone reproduction until growth is essentially completed. Our third assumption,
then, is that natural selection favors individuals that exploit opportunities to accelerate or maximize growth (Rubenstein [1993] presents models). Following all
three assumptions, we should expect immatures in focal taxa to act to maximize
their dominance status within whatever constraints are imposed by existing social
structure. Also, we should expect primate mothers to do whatever they can to help
maximize offspring dominance. Other behavioral options that reliably offset the
naturally low dominance status of juveniles should also be pursued (e.g., social
association, support, and alliances) [Pereira, 1988a; van Noordwijk et al., 19931.
Finally, if restricted time frames characteristically exist within the overall growth
period during which dominance can markedly promote growth, due to discontinuities of growth effort Le., spurts), special effort in dominance acquisition should be
timed to occur before or as they begin. In the absence of growth spurts, new efforts
in dominance acquisition may occur in conjunction with other major life-history
challenges (e.g., dispersal, group transfer, first reproduction).
Focal Taxa and Sources of Data
Among the Papionini, we consider the highly size-dimorphic savanna baboons
(Papio cynocephalus subspp.), the relatively nondimorphic rhesus and Japanese
macaques (Macaca mulatta; M . fuscata),and the moderately dimorphic longtailed
and toque macaques (Macaca fascicularis; M . sinica). While these three groups of
monkeys share pervasive similarity in life history and social system [Pereira,
1992; below], males differ in .their prereproductive development of dominance relations. I argue that divergent patterns of growth among these large Anthropoids
determine the extent to which adult females attempt to control the dominance
relations of immature males. The analysis recalls Jarman’s [ 19831 treatment for
large herbivores, illustrating that species often attain a given degree of adult size
148 I Pereira
dimorphism via disparate growth schedules and that species-typical growth profiles arguably interrelate adaptively with aspects of socioecology and mating system.
We consider next the ringtailed lemur (Lemur catta), a prosimian primate
sharing basic life-history features with the focal Papionini while also showing
important differences. Comparative study of such sociobiologically similar but
phyletically dissimilar species help us to identify potential cause-effect relations
among aspects of behavior, development, and ecology. Both ringtailed lemurs and
the focal Papionines form semiclosed,multimale-multifemale social groups among
which mature males transfer [Jones, 1983; Pusey & Packer, 1987; Sussman, 19911.
In each setting, agonistic relations among groupmates are mediated unambiguously by classical dominance relations [de Waal & Luttrell, 1985; Pereira & Kappeler, in press]. Mothers provide nearly all direct care for infants, including carriage across months of lactation [Klopfer & Klopfer, 1970; Altmann, 19801 and
mother-daughter bonds intensify as females mature and seek to integrate themselves among the adults of their natal groups [Pereira & Altmann, 1985; Pereira,
1993c; Pereira & Kappeler, in press].
Unlike the monkeys, ringtailed lemurs have short mating seasons and very
short, closely synchronized estrus periods [Jolly, 1966; Evans & Goy, 1968; Pereira,
1991; Sauther, 19911. In addition, ringtailed lemurs exhibit no body size dimorphism [Kappeler 1990a1, adult females invariably dominate males [Jolly, 1966;
Kappeler, 1990b1, and dominance relations among members of a given sex are not
always transitive [Pereira, 1993c;Pereira & Kappeler, in press]. Also crucial to our
analysis is that ringtailed lemurs respond to annual photoperiodic cycles to schedule not only their reproduction but also their growth and other life-history adjustments seasonally [Pereira 1993bl. I suggest that environmental seasonality maintains a particular neuroethological constraint that prevents ringtailed lemurs
from developing a system of rank inheritance like that of the Papionines, which in
turn further augments the importance of rapid growth and direct struggles for
dominance among infants in this species.
To minimize disruptive citation throughout the essay, many principal articles
on which it is based are cited here. Some data have long been available, such as
some of those on dominance development [e.g., Kawamura, 1958; Koford, 1963;
Sade, 1967; Cheney, 1977,1983; Lee & Oliver, 1979; Berman, 1980; Walters, 1980;
Datta, 1983a,b,c; Netto & van Hooff, 19861 and weight growth in Papionine monkeys [van Wagenen & Catchpole, 1956; Mori, 1979; Sugiyama & Ohsawa, 1982;
Coelho, 19851. Other information was published only more recently [e.g., Johnson,
1987, 1989; Turnquist & Kessler, 1989; Chapais, 1988, 1992; Chapais et al., 1991;
Strum, 1991; Altmann et al., 1993; Chapais & Gauthier, 1993; Pereira, 1988a,b,
l989,1992,1993b,c, 19941, and other data were heretofore unpublished (see figure
legends and Acknowledgments), including many of my own.
ACQUISITION OF DOMINANCE IN PAPIONINE MONKEYS
Basic Patterns
Most papionine females remain in their natal group for life, while the large
majority of their male peers disperse after maturing and seek to establish residency in nearby social groups [Pusey & Packer, 19871. As adults, closely related
females typically occupy adjacent ranks in their group’s hierarchy of dominance
relations, individually and collectively dominating Zowborn females (of lowerranking matrilines) while being dominated by highborn females (of higher-ranking matrilines). Several studies have demonstrated stability for matrilineal dominance hierarchies exceeding a decade [reviewed by Pereira, 19921, stability so
Development and Dominance Among Primates I 149
reliable, it appears, that females adjust offspring sex ratios in relation to their
matrilineal status [van Schaik & Hrdy, 1991; see also de Waal, 19931. Whereas
many young males probably transfer into groups containing brothers when possible, no standard, systematic effects of kinship on male dominance relations are
known. Instead, adult males depend heavily on their size and independent agonistic prowess to acquire dominance [e.g., Hausfater, 1975; Sugiyama, 1976; van
Noordwijk & van Schaik, 1988; Hamilton & Bulger, 1990; Sprague, 19921.
Observational work on development revealed both expected similarities and
unexplained differences between the dominance system of rhesus and Japanese
macaques, which was studied first, and that of savanna baboons (Fig. 1). As in the
macaques, male and female baboons came first to dominate particular age peers as
infants, then overturned certain older immatures a s juveniles, and finally overturned certain adults only after having approached puberty. As in juvenile
macaques of both sexes, juvenile female baboons outranked one another according
to maternal rank and became dominant to only the lowborn among older females.
By contrast, juvenile male baboons consistently outranked all female peers and
outranked one another according to age or size, irrespective of matrilineal membership. In addition, young male baboons achieved dominance over older highborn
as well as lowborn females, typically overturning even several highborn adult
females well before puberty. Other immature Papionines, by contrast, were very
rarely ever observed to contravene the aforementioned patterns by “overachieving” in rank acquisition. Exceedingly few females, for example, ever targeted older
highborn females for rank reversal [Netto & van Hoof, 1986; Walters, 1980;
Pereira, 1989, 1992; Chapais, 19921.
Mechanisms
Understanding ontogeny entails identifying mechanisms, and real progress
has been achieved in this area for papionine rank acquisition and maintenance.
Conjointly, field and laboratory work have emphasized the importance of social
cognition and patterned adult female intervention into juveniles’ conflicts. In research on Amboseli baboons, for example, female intervention was differentiated
by juvenile sex (Fig. 2). Relatively high-ranking females intervened relatively
frequently in immature females’ conflicts with other females and invariably to
support the highborn animal, juvenile or adult [Walters, 1980; Pereira, 19891.
Those same adults, by contrast, intervened in young males’ conflicts infrequently
and supported males without regard to rank relations between the matrilines of
males and their opponents [Pereira, 1989; see also Netto & van Hooff, 19861. The
systematic adult intervention into juvenile females’ conflicts both ensured and
limited them to the acquisition of matrilineal dominance rank. The juvenile males,
by contrast, were comparatively free to antagonize and ultimately dominate highborn females [Pereira, 19921.
These results revealed that baboon females recognize not only the sex of juvenile individuals, but also their matrilineal membership and the relative dominance status of their matriline. They also suggested that systematic adult female
agonistic intervention, according to existing dominance relations among matrilines, is the principal mechanism underlying the inheritence and stability of dominance rank for these female monkeys. Experiments with other Papionines in
captivity confirmed and extended these interpretations. By having them distinguish pairs of photographs showing related vs unrelated groupmates, Dasser
[19881 showed that female longtailed macaques ( M . fusciculuris) recognize allies
within their groups. And, by removing and replacing related and unrelated sources
of agonistic support, Chapais [19881 and colleagues [Chapais et al., 19911showed
150 I Pereira
ADULT
FEMALES
i
7 @ 2
8
m
5
418217
ID4
JUVENILES
2 @ 6
6
birth
order
Rhesus /Japanese
Macaques
mo Ihe r ‘s
rank
0
1
birlh
order
Savanna
Baboons
Fig. 1. Schematic illustration of papionine species differences in juvenile dominance relations. Males are
represented by squares, females by circles. Matriarchs have double-letter acronyms, and their daughters’ numbers indicate birth order; three-character acronyms identify matriarchs’ grandoffspring. Adult females invariably outrank all young juveniles in dyadic interactions. Juvenile male and female rhesus and Japanese
macaques outrank one another according to maternal rank, whereas juvenile male baboons outrank all female
peers and outrank one another according to age.
that the inheritance and maintenance of matrilineal dominance rank in female
Japanese macaques depends on the hierarchy-reinforcing patterns of intervention
that characteristically occur among them. More recently, these researchers detailed how Japanese monkeys first experience systematic adult female intervention long before weaning [on other spp. see Berman, 1980; Datta, 1983a,c;Horrocks
& Hunte, 19831 and showed that infants learn to behave dominantly toward lowborn groupmates partly by observing their mothers do so [Chapais & Gauthier,
19931. Our interpretation of all of these studies is corroborated by the common
observation of persistently unstable dominance relations among unrelated adult
females in artificially composed groups of captive macaques.
Given the great similarities in life history and social structure between
Development a n d Dominance Among Primates / 151
T
i
% Interventions Reinforcing Hierarchy
Fig. 2. Pattern of adult female intervention in agonistic interactions ofjuvenile male (top) and female (bottom)
savanna baboons. Bars indicate, in relation to sex of opponent, percentages of support to juveniles that reinforced
existing hierarchy of dominance relations among matrilines.
macaques and savanna baboons, observed differences in the ontogeny of male
dominance relations offer a n opportunity to explore relationships between the
development of primate individuals and that of their social systems. Heretofore,
well-justified focus on female development led to relative neglect of issues surrounding male development. One perspective that emerged was that adult females
can be expected to be less involved in young males’ rank relations because males
are destined to disperse [Pereira, 1989; Lee & Johnson, 19921. Successful development, however, is a t least as important to sons as to daughters across the years
preceding their dispersal, and existing data suggest that adult female macaques do
promote matrilineal rank acquisition by juvenile males. Why then do female baboons promote rank acquisition only for females against other females? Why do
immature male baboons invariably dominate their female peers? And why do they
relatively easily come to outrank even highborn adult females? My attempt to
provide answers to these questions begins with a n examination of papionine size
dimorphism and the manner in which it develops.
G r o w t h patterns and adult agonistic relations. Anthropoid primates
schedule growth and achieve size dimorphism differently than do most other animals. Virtually all nonprimate endotherms exhibit maximal growth rates shortly
after birth and progressive decline in growth rate beginning around the time of
sexual maturation [Brody, 1945; Pereira, 1993al. In size-dimorphic species, members of the larger sex are typically somewhat larger at birth and grow faster
postnatally than those of the other [e.g., Jarman, 1983; Ricklefs, 1983; McLaren,
19931. In large anthropoids, by contrast, growth rates decline after rapid neonatal
growth and remain suppressed until puberty, when the males in most species and
females in some show a disinhibition termed the “adolescent growth spurt” [Watts,
1985, 1986; Leigh, 19921. Large samples of neonatal or juvenile weight data typically reveal the average male to be slightly heavier than his average female
counterpart, but these differences are exceedingly small and accompanied by great
variability.
152 J Pereira
Two important points emerge here. First, immature papionine females are
slightly larger or smaller than individual male peers in any given social group as
a result of their birth dates. Second, juvenile males and females remain much
smaller than adults for years. It is also likely that juvenile nutritive requirements are considerably smaller than those of reproducing females, due to both
size differences and the relatively small energetic allocations juvenile Anthropoids make toward growth [Janson & van Schaik, 19931. Considering these factors
alone, we likely explain why cercopithecine adults, male and female, dominate
all young juveniles on independent bases (i.e., apart from third-party effects;
Fig. 1).
Following puberty, male rhesus and Japanese macaques in the best-known
free-ranging populations outweigh females by 15-30%, on average. By contrast,
mature male savanna baboons typically weigh 80-100% more than do adult females. Associated with this difference are significant contrasts in adult social
relations. The adult female macaques, for example, readily collaborate to attack
adult males. Moreover, some females independently dominate some adult males,
and high-ranking females can influence male dominance status and group membership [reviews by Smuts, 1987; Pereira, 19921. In contrast, agonistic coalitions
by adult female baboons against males are rare and ineffective [Packer & Pusey,
19791, adult male baboons invariably dominate individual females, and there s no
known effect of maternal rank on the dominance relations, migration patternj, or
reproductive success of male baboons [Altmann et al., 19881.
In sum, compared to their macaque counterparts, adult male baboons are so
large a s to be agonistically unassailable from the viewpoint of adult females,
whereas this taxonomic difference is not manifest among juveniles, where females
are as large a s males, regardless of species, and all are smaller than adult females.
Large juvenile male size, then, cannot explain taxonomic differences in the development of males’ dominance relations [cf. Lee & Johnson, 19921. On purely physical grounds, young juvenile male baboons are as easy for adult females to coerce
and socialize as are young juvenile male macaques.
Pubertal development and prior female control of juvenile males. Female primates should promote offspring dominance whenever feasible to help maximize offspring access to nutriment during difficult foraging periods and, especially, critical growth periods. In the relatively nondimorphic species, mothers can
and do help sons and daughters alike to dominate lowborn male and female peers,
thereby maximizing their chances for survival, extensive growth, and early reproduction [e.g., Drickamer, 1974; Paul & Thommen, 1984; see also Rubenstein,
19931. In baboons, by contrast, adult females support neither sons nor daughters
over lowborn male peers. This, I suggest, is because the required agonistic interventions are too risky for these adult females when they matter most, just before
and a t puberty.
The dramatic pubertal growth spurt in baboons can generate a doubling of
male body weight in just over 2 years, whereas pubertal female baboons show little
to no acceleration of weight growth. In rhesus and Japanese macaques, by contrast,
the substantial male growth spurt is paralleled by a more moderate pubertal
acceleration of female growth, such that average sex differences in adult weight
are comparatively modest. The growth capacity of maturing male baboons, therefore, exceeds that of their macaque counterparts relative to the nutritive requirements of conspecific females. All else equal, maturing male baboons should comPete more aggressively, against peers and adult females, over access to food.
Inadequate nutrition could jeopardize their health and reduce adult body size,
compromising their potential for long and effective reproductive careers. Even if
Development an d Dominance Among Primates / 153
growth can be postponed in response to nutritive shortage, age at first reproduction
would be compromised [Hamilton & Bulger, 19901.
Direct comparison of papionine growth trajectories, in fact, suggests several
related factors that should encourage and help maturing male baboons to compete
relatively aggressively against females (Fig. 3). Along with the near absence of a
female growth spurt, males in this species attain a much larger proportion of adult
female size before initiating their spurt (-82%) than do male rhesus ( - G O % ) ,
increasing for them the viability of aggressive tactics a s puberty approaches. Also,
the potential for continued growth after puberty seems reduced for both sexes in
baboons in comparison to macaques [see also Leigh, 19921. Two predictions deserving attention in future research, then, are that successful foraging is more important, and aggressive competitive tactics more prominent, in maturing male baboons than in their rhesus or Japanese macaque counterparts. In my own research,
food was at stake in most juvenile male but not female aggression toward unrelated peers and adult females, and males were five times more likely than females
to use contact forms of aggression [Pereira, 1988bl.
Now, most macaques breed seasonally, while most baboons do not [Lindberg,
19871. If seasonality exacerbates feeding competition among mothers or their
weanlings [e.g., Wasser & Starling, 19881, females might be favored that maintain
as much agonistic influence over males as possible [Jolly, 19841. “Male dominance” among juveniles in the most dimorphic seasonally breeding Papionines,
however (Fig. 41, suggests that growth patterns, not environmental seasonality,
primarily determine the degree to which females constrain juvenile male dominance relations [on Barbary macaques, M. syZuunus, see Kuester & Paul, 19881.
This may also hold among Cercopithecini, where DeBrazza’s monkey (Cercopithecus neglectus), the most dimorphic guenon, may show general male dominance
among juveniles [preliminary data in Kirkevold & Crockett, 19871, whereas the
less dimorphic vervet monkeys ( C . uethiops) exhibit the rhesus/Japanese macaque
pattern of matrilineally ordered dominance relations among all juveniles [Cheney,
1983; Horrocks & Hunte, 1983; see also Cheney, 1977 on the relatively nondimorphic chacma baboons, Pupio c. ursinusl.
Females in cercopithecine taxa showing relatively great adult size dimorphism, then, appear not to help daughters maintain dominance over lowborn male
peers, and, in the extreme case of savanna baboons, neither do they assist sons. The
most dimorphic macaques constitute cases of intermediate papionine size dimorphism, and mothers in these species appear to provide intermediate levels of assistance: static data (Fig. 4) suggest that they help primarily sons maintain dominance over lowborn male peers. Our uncertainties here are due to the fact that all
of the crucial types of data on adult intervention into juvenile conflicts-classified
by not only matrilineal membership, but also sex and role ofjuvenile and opponent
and type of intervention and response [discussion in Pereira, 19921-have not been
published for macaques of any kind [for a variety of other detail on intervention
behavior see Datta, 1983a,b,c; Bernstein & Ehardt, 1985; Netto & van Hoof, 1986;
Chapais, 1988; Chapais et al., 19911.
A simple algebraic model accounts simultaneously for effects of pubertal male
size and potential for growth relative to females:
Here, female agonistic effort to control juvenile male dominance behavior, Cf,
relates inversely to the product of relative male size a s the growth spurt begins, S ,
(proportion of adult female size), and potential for male growth during puberty, G,
Rhesus Macaques
--
/ - I
I
I
h
M
e.
Longtailed Macaques
7-
74% increase
a4
.-
Be
3
2
2
3
I
0
25
1
2
3
5
A
-
I
I
4
6
/
n
7
8
7
8
I
M
c 20
9
C
10
5
0'
-.
0
I
1
2
3
4
1
5
6
Age (yeam)
Fig. 3. Patterns of growth in Papionines showing relatively slight (top),moderate (middle), and great (bottom) adult size dimorphism. Infants are weaned in each taxon around or before 1 year of age. Beginnings and
ends of pubertal male growth spurts were taken directly from associated growth velocity curves in each original
dataset [rhesus: van Wagenen & Catchpole, 1956; longtails: van Schaik e t al., unpublished data; see also Janson
& van Schaik, 1993; baboons: Coelho, 19851. Using data from captive, provisioned representatives of each species
allows comparison of maximal male growth capacities. S, highlights proportions of prime adult female weights
comprising male weights a t outsets of pubertal growth spurts (see text). G, for each taxon is proportion of male
size increase divided by duration of growth spurt (e.g., rhesus: 1.0712.3).
Development and Dominance Among Primates I 155
4 yr-olds 3 yr-olds
.
Timsel
Group
uE
Group A
Group D
Fig. 4. Juvenile dominance relations in two relatively dimorphic macaque species (adult maldfemale weight
ratio approximately 1.50).Timsel Group of longtailed macaques (M.
fascicularis, Sumatra) [van Noordwijk,
unpublished data]. Groups A and D of toque macaques (M.
sinica, Sri Lanka) [Baker, unpublished data; also
Baker-Dittus, 19851. Juveniles' matrilineal ranks shown in symbols; individual identities in subscript. Threeyear-old male longtail KL dominated both four-year-oldsin his group.
(maximal proportion of size increase divided by duration of spurt). This model
renders predictions on physical or behavioral development for any macaque or
savanna baboon population, including any of our focal taxa characterized by different degrees of prime adult weight dimorphism from those cited here (without
obesity; see Pereira and Pond [19951 on variable tendencies toward obesity within
primate genera). Taking data from Figure 3, for example, the index predicts relatively great female control of juvenile male rhesus macaques (Cf -4.51, relatively
low female control of young male baboons (Cf -3.11, and intermediate female
control of young male longtailed macaques (Cf -4.0) [for cross-sectional cumulative weight growth data in M. sinica see Cheverud et al., 19921. Current knowledge
suggests that when the relative size and growth capacity of pubertal males reduce
this index toward the baboon value, adult females operating in a multimale papionine social system stop trying to control the ontogeny of male dominance relations altogether.
Canalized cognition of sex-typical behavioral attributes? Papionine females' perspectives on agonistic interaction with mature males clearly vary in
accord with species-typical dimorphism and schedules for its development. These
are taxonomic differences in social cognition-female cognition of males and their
agonistic attributes, presumably complemented by differences in male cognition
(e.g., below). An intriguing question that remains asks what mechanisms underlie
the development of taxonomic differences in the sexes' perceptions of themselves
and one another. I argue, for example, that male baboons' great pubertal size and
growth are paired functionally with great motivation to outcompete others for food
and that females who try to compete with maturing males more often incur injuries than females doing so in less dimorphic taxa. This alone could cause female
baboons to develop a disinclination to fight with mature males.
But what causes baboon females not to fight with juvenile males? Three datasets suggest that female baboons may have somewhow evolved a general disinclination to interact aggressively with males. First, baboon mothers do not assist
even young juvenile offspring in dominating male peers. One might argue that this
156 I Pereira
simply reflects that dominance among juveniles functions not to mediate resource
access, but rather to establish precedents in relations that become important
around maturation. This inference is, in fact, supported by both the seeming lack
of immediate cause for many juvenile conflicts [Pereira, 1988b; Johnson, 19891 and
the new theoretical perspective on slow anthropoid growth [Janson & van Schaik,
19931. On the other hand, mothers assist all or some offspring to dominate male
peers in all other well-known Papionines, and other data considered in this work
also support the prediction that female primates typically help to maximize offspring dominance.
Second, in all relevant data reported to date, juvenile males’ efforts to overturn
adult female baboons in dominance are found to have been resisted only weakly in
comparison to those of juvenile females. Indeed, amusing sights during my own
fieldwork involved several relationships in which tiny 2-year-old males independently elicited submissive signals from much larger mature females. Finally, in all
research examining juvenile male-female relations in highly dimorphic baboon
populations, females have ceded dominance to males of roughly the same size [cf.,
Cheney, 1977 on Pupio c. ursinus].This has occurred almost invariably despite the
facts that immature female baboons are not systematically punished by adults for
fighting with young males [Pereira, 19891, many actually exceed particular male
peers noticeably in size, and many are members of higher-ranking families [e.g.,
Pereira, 1988bl. The consistency of these observations, among age classes and
study sites, suggests that female baboons perceive males per se as inappropriate
targets for solo agression and that this perception is stabilized remarkably early in
life.
The mechanism may lie instead with male behavior. Males in dimorphic species might have evolved an orientation toward forming agonistic alliances with one
another, for example, because females cannot safely assist them in fights with
other males. In Amboseli, juvenile males received agonistic support as often as did
juvenile females, and their support came predominantly from male peers and older
immature males [Pereira, 19891. Also, adult male coalitions are a prominent feature of savanna baboon natural history; data on them outstrip those on any other
coalitions among unrelated primates [Noe, 19921. Far fewer data on male-male
coalitions have accumulated, by contrast, in the voluminous literature on rhesus
and Japanese macaques [e.g., Watanabe, 1979; Bernstein & Ehardt, 1985; Sprague, 19921, whereas the other Papionine well known for intragroup male-male
alliances is one of the more dimorphic macaques (bonnets, M.rudiutu) [Silk 1993bl.
Of course, both things may be true: male baboons might be predisposed to form
agonistic coalitions, while female baboons are naturally inclined not to fight with
males. But also a less adaptationist developmental cascade remains equally viable.
All developing cercopithecine males exhibit some social affinity [Fairbanks, 19931,
In baboons, young males’ older associates are unusually formidable allies, as discussed earlier. Female baboons may simply learn early on that conflict with even
one young juvenile male often leads to an undesirable tangle with one or more
much rougher ones. As these females learn consequently not to fight with males,
males learn that it is easy to harass and out-compete females, especially when
acting together.
This hypothetical ontogenetic cascade posits for baboons neither evolved female predispositions to avoid conflicts with males, nor unique male predispositions
to collaborate. It remains one, however, that, in conjunction with common patterns
of association and species-typical patterns of growth, could promote cognition of
sex-typical agonistic capacities that is taxonomically extreme. Male and female
perceptions of one another throughout development would stabilize observed adult
Development and Dominance Among Primates I 157
modes of male-female interaction, which in tu rn would promote parallel sex-typical behavior among immatures. We should continue to respect the possibility that
all three mechanisms discussed have, in fact, come into play over evolutionary
time, providing the mechanistic redundancy characteristic of integrated life history traits. Before dismissing out of hand possible roles for predispositions in agonistic relations between the sexes, one should reflect on accumulating data regarding the evolution and development of “female dominance” in ringtailed
lemurs.
ACQUISITION OF DOMINANCE IN RINGTAILED LEMURS
We t ur n now to ringtailed lemurs (Lemur catta), the prosimian primate for
which several aspects of life history, including social structure, most closely resemble those in the papionine taxa (see Introduction). The following overview
combines heretofore unpublished data with others recently presented elsewhere
[Pereira, 1993b,cl.
Basic Patterns
Adult and adolescent ringtailed lemurs invariably dominate all younger group
members, and all juveniles dominate all infants [Pereira, 1993c, 19941. In my 9
years of research at the Duke University Primate Center (DUPC), infant ringtailed lemurs have invariably established dominance relations among themselves
by 4-5 months of age, 1-3 months before weaning (data from 16 cohorts). Also,
birth peers’ dominance relations have always been transitive and completely stable, barring illness, until maturation. Infants generally outranked their lighter
peers [Pereira, 1993~1,and neither infant sex nor small age differences (<3 weeks)
nor maternal weight o r dominance status affected either weanling weight or dominance rank. Large age differences, however (>3 weeks), invariably did: infants
conceived during second or later sets of estrous cycles during mating seasons [see
Pereira, 19911consistently have the lowest weaning weights and dominance ranks
in their cohorts. Eight of nine such youngsters born before 1992 showed belowmedian body weights and dominance ranks in their cohorts by puberty.
Puberty in ringtails occurs around 15 months of age at the DUPC and around
26 months at Berenty, as evidenced by testicular enlargement and the onset of
genital scent-marking [Jones, unpublished data; Pereira, unpublished data]. At
both study sites, dominance relations changed around puberty, both among adolescents and between adolescents and adults [Pereira, 1993c, 19941. The invariant
ringtailed lemur phenomenon of mature female dominance over all males began to
emerge gradually a t this time, and adolescents’ agonistic relations with adult
females also differentiated: only maturing females were included in the seasonal
phenomenon of targeted aggression. During premating and birth seasons, mature
and maturing females in the DUPC and Berenty populations spontaneously target
female adversaries for persistent, intense aggression that can result in dominance
reversal, infanticide, and/or social eviction Wick & Pereira, 1989; Koyama, 1991;
Pereira, 1993c, 1994; Pereira & Kappeler, in press].
Mechanisms
Adult female intervention in immatures’ conflicts. Since the dominance
relations of immature ringtailed lemurs do not correlate with maternal attributes
and rarely change before puberty, juvenile ringtailed lemurs do not systematically
“inherit” dominance as do juvenile papionine monkeys [Pereira, 1993~1.Quantitative behavioral observation corroborated that adult female ringtails make no
patterned effort to influence the dominance relations of offspring. In my initial 15
158 I Pereira
Fig. 5. Adult female intervention in conflicts of juvenile and adolescent ringtailed lemurs consistently promoted neither inheritance of maternal dominance status (top four bars) or female dominance over males (bottom
bar). All interventive aggression was moderate to severe (i.e., caused victims to jump away or flee). Top bar:
Maternal intervention vs. age peers. Second bar: Maternal vs. adult females. Middle bar: Nonkin intervention
vs. all opponents. Fourth bar: Nonkin intervention into only immature females' fights, against all opponents.
Bottom bar: All adult female intervention between females and males.
month study, for example, only eight of 26 immature subjects ever received maternal support against peers, and six of these eight received such support only once
[Pereira, 1993~1.In addition, maternal aggressors dominated their offsprings' opponents' mothers in only 50% of interventions (Fig. 5). Moreover, immatures never
responded to maternal support by rejoining to coattack their former aggressor,
which is a crucial aspect of rank acquisition for Papionines [e.g., de Waal, 1977;
Walters, 1980; Pereira, 19891. Finally, agonistic intervention by nonkin females
also was not patterned in ways that could have promoted either inheritance of
maternal dominance status or the development of female dominance in this species
(Fig. 5). In spring 1994, a long-term bottom-ranking adult female in one study
group overturned the matriarch and all three of her adult daughters, providing
dramatic testimony to the fact that female ringtails do not act to promote or secure
the dominance of kin.
Competition for dominance among infants. In most dyads, dominance relations appeared to be settled through experience in rough-and-tumble play, as
this was virtually the sole mode of nonfilial social initiative exhibited by infants
[also Gould, 19901. But also, intense grappling commonly erupted spontaneously
between 3-month-old infants that were very closely matched in age or size (Table
I), and grapples never occurred between infants more than 40 days apart in age.
Most grapples broke out during wrestling play rather than foraging, and all sent
combatants to the ground, where they bit each other violently about the head and
shoulders and raked one another with their feet. When nearby adult females noticed grapples, they typically charged any noninfant within about 5 m (n = 14).
More rarely (n = 51, females (n = 3) attempted to intervene, but, none was ever
aggressive toward either grappler. Each nonalpha female that attempted to intervene (one/group) was attacked immediately by a dominant female.
Grappling clearly established dominance relations (Table I). In many pairs,
two or more grapples have been observed over a 1-2 week period. Clear winners
Development and Dominance Among Primates / 159
TABLE I. Relative Age Differences
and Ultimate Dominance Rank Differences
Between Grappling Infant Ringtailed Lemurs
Rank differences
1
Relative age difference”
Dominance rank difference
at weaning
2
3
4
5
1
4
4
1
1
1
1
2
4
0
0
0
“Infants of each cohort ranked by age; grapplers’ differences in
age rank shown; whereas similarities in weight may have exceeded similarities in age [Pereira, 1993~1,birth cohorts could
rarely be weighed close to days of grapples.
(n = 8 before 1993)remained a t conflict sites, taking over no resource, while their
opponents ran to their mothers [also Pereira, unpublished data]. During subsequent play or conflict over food or partners, grapple winners readily intimidated
former opponents, eliciting the species’ vocal signal of subordination (“spat” call
[Pereira & Kappeler, in press]). In almost all cases, grapplers subsequently occupied adjacent dominance ranks (Table 1)[Pereira, unpublished data].
Changes at puberty and targeted aggression. In every year of my research, fully mature adults have been the first males seen to issue submissive
signals to maturing females, always before mating began and almost invariably in
the absence of female aggression (1985-1994). Females’ dominant male peers, by
contrast, have typically become submissive only by the end of pubertal mating
seasons. Thus, female sexual maturation seems to induce a change in mature
males’ perception of young females, leading males spontaneously to behave submissively to them. We have suggested evolution via sexual selection [Pereira et al.,
1990; Pereira, 1991; Pereira & Weiss, 19911, with females accepting only submissive males as mates, thereby ensuring their own access to food in a harshly seasonal, semiarid environment. Female dominance in ringtailed lemurs, in that case,
would reside in mature male neurophysiology. Irrefutably, males do not feel compelled to submit unconditionally to female peers until they fully mature themselves [Pereira, 1993~1.
One or more females in four of five adolescent cohorts in my initial study of
ringtailed behavioral development were selected by adults for targeted aggression,
and long-term data showed that maturing females had to overturn some adult
females in dominance t o remain in large or growing natal groups [Pereira, 1993~1.
Maturing females received agonistic support primarily from their mothers (Fig. 5)
and also significantly increased their own rates of intervention in adult female
conflicts (Fig. 6). Unexpectedly, however, no evidence suggested that mature females sought actively to influence the dominance relations of kin. Maternal intervention was not only rare (mean: 0.6%of all conflicts), it was also unpatterned
in relation to maternal dominance relations (Fig. 5). In addition, neither juvenile
nor maturing females showed greater anticipation of maternal support than did
male peers. Despite receiving more adult aggression, for example, adolescent females took no greater responsibility than did their male peers for time spent near
their mothers, and only young juveniles-male and female alike-markedly increased rates of filial approach in response to adult female aggression [Pereira,
1993~1.Finally, following seasons for targeted aggression and their associated
rank reversals, ringtailed mothers and their mature daughters often did not dominate the same sets of female groupmates (Fig. 7).
160 I Pereira
males
"
.....
""
juvenile
adolescents
Age Class
Fig. 6 . Ontogeny of agonistic intervention in immature male and female ringtailed lemurs. At puberty, females
radically increase their rates o f intervention in adult female conflicts, while males continue to intervene in
others' fights only rarely.
Seasonality, synchrony, growth, dominance, and aggression. Lemur
rates and scheduling of growth contrast sharply with known anthropoid phenomena [Kirkwood, 1985; Kappeler, 1992; Pereira, 1993bl. Though their mothers were
a n order of magnitude smaller than most papionine females, for example, infant
ringtails grew as fast or faster than do infant Papionines, gaining 4-8 g of body
weight per day, on average, across their first 7 months [Pereira, 1993bl. Thus, the
ringtailed infants attained about 35% of average adult weight by weaning,
whereas infant Papionines achieve only about 25% of adult female weight by
weaning (Fig. 3) and take at least twice a s long to do so.
After the first half of lactation (0-3 months), ringtailed infants entered a 4-5
month period, extending beyond weaning (approximately 6 months of age), during
which growth rates remained high (moderate provisioning: X = 4.6glday; n = 10)
or accelerated (heavy provisioning: X = 7.5 glday; n = 5; F = 9.19, P < 0.01).
Next, around their eighth month, juveniles invariably exhibited sudden, substantial reductions in growth rate (65-75%), regardless of provisioning level, and
growth remained suppressed for the next 5-7 months [Pereira, 1993bl. Twelve
months after youngsters' first summer of rapid growth, 15-20-month-old immatures matured sexually and experienced 3-4 consecutive months of elevated
growth rate.
These and other data [Pereira, 1993bl revealed basic photoperiodic control of
growth rate, and possibly also social behavior, in relation to predictable seasonality of nutrition in the wild. Very high rates of growth occurred opportunistically
during and just after the photoperiod of the rainy season in southern Madagascar
(Fig. 8). All grapples to establish dominance relations were observed a t the outset
of this period, beginning just after the summer solstice, when infants began helping to sponsor their own rapid growth (Fig. 9). Growth rates were invariably
suppressed thereafter across most of the photoperiod of the southern harsh season.
Campaigns of targeted aggression were also abandoned at this time, each year
Development a n d Dominance Among Primates / 161
0
n
Lcl
@a
@ Group
Lc2
Group
T
Group
a
Fig. 7. Stable, intransitive dominance relations among mature females in three study groups of ringtailed
lemurs. Lcl and Lc2 groups a t DUPC (1989-1990); T group at Berenty Reserve (1992). In each case, females
dominated all those listed beneath them for several consecutive months, except where upward arrows show
low-rankers that stably dominated otherwise topranking female (see Fig. 1for acronym scheme). Each subscript
a identifies adolescent female; each subscript y indicates individual independently estimated to be youngest
among mature females (by author and two other fieldworkers). Numbers to left of T group identify three cliques,
as defined by mutualistic association and grooming patterns. In Lcl and Lc2 groups, such cliques include all
motherdaughter pairs.
when female adversaries had failed to evict one another [Vick & Pereira, 1989;
Pereira, 1993~1.
Physical and behavioral development in ringtailed lemurs have coevolved in a
social context in which adult females reliably fail to intervene to determine the
outcomes of immatures’ conflicts. Thus, infant ringtails seem to grow fast to become dominant to continue growing fast, before markedly reducing growth effort
and engaging their first long harsh season. Rates of growth and probably metabolism [Pereira 199313, 19941 are inevitably substantially suppressed for most of
their dry season. By maximizing size, youngsters maximize their capacities in
foraging, competition, and fat storage, which conjointly help to minimize risk of
dry season mortality [Pereira 1993a,b; Pereira & Pond, 19951. The paramount
importance of extensive infantile growth is corroborated firmly by the accelerated
and extended growth characteristic of late-born infants. Growth rates of semiindependent late-born infants exceeded those of older infants in 7 of 8 months prior to
autumnal reductions (Septembers and Octobers, excluding October, 1993), and in
9 of 10 months following reductions (Table 11) (rapid growth one month is typically
followed by relatively slow growth the next, so it is conservative to treat consecutive months as independent data points in these comparisons). Analysis of effects
of age vs. size using an entire 6 year database revealed that it is small size, not
young age, that delays the reduction of growth rates in the autumn [Pereira,
1993131.
Relationships among infant growth rate, dominance, and survivability have
probably influenced life-history evolution in ringtailed lemurs. While mating seasons in many group-living primates are well defined, for example, few are so
sharply delineated a s those of ringtailed lemurs, where female groupmates typically all conceive within 7-20 days of one another [Jolly, 1966; Pereira, 1991;
Sauther, 19911. I propose that reproductive synchrony among female ringtailed
162 i Pereira
10
FE
WS
SE
F E W
120
- 6 4 l l 4 l - T
1 2 3 4 5 6
Month of Life
Fig. 8. Mean growth velocities across the first 2 years of life, under high provisioning (solid line) and moderate
provisioning (dashed line), for infants whose births were clustered between the end of March and April. Solstices,
equinoxes, and sample sizes indicated. Mean monthly rainfall values for the same photoperiods in southern
Madagascar (dotted line).
lemurs functions to rule out insurmountable size advantages among neonates
about to race for the size needed to convey dominance [for detailed analogy on rate
of embryonic development, hatching synchrony, and nestling competition in birds
see Ricklefs, 19931. In turn, birth synchrony feeds back to reinforce the developmental patterns of frequent rough play and agonistic grappling, as necessary,
among infants to establish dominance relations.
Size differences around weaning should have far-reaching effects among
healthy survivors because immatures’ dominance relations typically remain stable
and should affect development continuously. Maturation rates on three “planes” of
nutrition predict that dominant juveniles mature faster. Provisioning enhances
development at the DUPC [Pereira, 1993b1, where almost all females bear their
first infant a t 2 years of age. At Berenty, by contrast, only a few females produce
their first infant at the age of 2 years [Jolly & Koyama, personal communication],
and, on still lower nutrition at Beza-Mahafaly, some 3-year-olds fail to produce
their first infant [Sussman, 1991; Sauther, 19921. By enhancing growth and nutrition, dominance may also help juveniles to develop superior agonistic capacity
by puberty. In large Duke study groups, only females that overturn adult females
in dominance secure reproductive positions [Pereira, 1993~1.Whereas maturing
males are not involved in targeted aggression, they disperse and must overcome
intense aggression by males resident in other groups before successfully immigrating [Sussman, 1991; Pereira & Weiss, 19911.
Development an d Dominance Among Primates / 163
I 0No.Grapples
-A-
Growth Rate
-
Time Feeding
1
Fig. 9. Codevelopment of growth rate, self-feeding, and agonistic relations in infant ringtailed lemurs. Juxtaposition of timing of grapples (n = 27, 1981-19901, average infantile growth rate (1986-1992), and mean
percentage time spent feeding (seven 1992 infants). As infants begin to contribute significantly to their own
nourishment, rates of growth often first decline, then accelerate IPereira, 1993b1, and intense mutual aggression
commonly erupts during play between infants that are very closely matched in size (see also Table I).
Why No R a n k Acquisition?
Especially on seasonal bases, female ringtails commonly intervene in others’
fights, and, in so doing, they sometimes shield kin from aggression. But, overall,
characteristic patterns of intervention seem to represent principally individual
opportunism, each female essaying to overturn, harass, and potentially evict her
own adversaries [Pereira, 1993c; Pereira & Kappeler, in press]. Why do female
ringtailed lemurs not genuinely collaborate to promote kin and stabilize hierarchical relations? By doing so, powerful females could help their matrilines dominate others, grow larger [Taylor, 1986; Vick & Pereira, 19891, and maintain their
ranges [Koyama, 19911, thereby enhancing reproductive success. So reasoning, in
fact, I predicted at the outset of my research that female ringtails would show the
same patterns of intervention as do papionine females. Especially given the mutualistic advantages of the papionine system [Chapais, 1992; Pereira, 19921, I
continue to believe that female ringtailed lemurs would effect “top-down” agonistic
intervention, if they could.
Why can’t they? To do so, females must be able to recognize group mates
visually, identify allied subgroups (e.g., mother-daughter pairs), and remember
the directionality of dominance between them. Forest-living ringtailed lemurs
present abundant evidence of visual recognition daily, including female targeting
of specific adversaries and male repulsion of potential immigrants [Pereira &
Weiss, 1991; Pereira, 1993~1.During many episodes, however, I have also seen
aggressors err, sprinting to attack and suddenly stopping after starting toward the
wrong animal (Table 111) [Pereira, unpublished data]. Almost invariably, mistaken
164 I Pereira
TABLE 11. Autumnal Growth Rates of Clustered and Individual Late-Born infant
Ringtailed Lemurs*
Birth date”
September
October
November
December
7.00
6.20
(1.66)
[31
9.90
5.83
(2.33)
161
4.10
1.34
(1.72)
171
3.90
2.94
(0.89)
28 June
20 March
7.90
5.80
(0.00)
[41
6.30
8.98
(2.48)
141
7.80
3.55
(0.98)
141
3.30
0.20
(2.03)
[41
7 June
22 March
7.50
7.29
(2.15)
[91
NA
4.50
2.80
(0.67)
[91
NA
22 June
9 April
3.70
3.45
(1.55)
[61
6.20
5.29
(3.46)
161
3.70
1.38
(2.43)
161
2.00
2.25
(0.75)
[41
17 May
17 March
10.50
6.45
( 1.40)
4.10
1.13
(1.13)
1.20
0.24
(0.86)
“71
“71
5.80
2.31
(0.83)
171
1986
Late-born
Others
10 July
10 April
“71
1987
Late-born
Others
1989
Late-born
Others
1991
Late-born
Others
1993
Late-born
Others
[51
*Grams per day; means, standard deviations (in parentheses), and sample sizes (bracketed) shown for clusters
of infants born at normal time each year.
aAverage date of birth shown for clusters of infants born at normal time of year.
targets have been, also to my eyes, among the group members most closely resembling known adversaries. Ringtailed lemurs appear least able to recognize groupmates reliably when they are first noticed fighting or otherwise moving rapidly. It
is probably for this reason that the targeted aggression phenomenon so prominently features aggressors’ a s well as victims’ constant monitoring of one another’s
locations and activities. Whereas lemurs evidently recognize one another by scent
(e.g., Table 111) and sound [Macedonia, 19861, neither capacity can ensure that
razor-sharp canine teeth applied to one of two whirling bodies would not injure the
intended beneficiary. And, in my experience, much higher proportions of escalated
dyadic conflict in lemurs than in papionine monkeys involves full-scale grappling,
with all eight hands and feet and both mouths attached between opponents.
On the basis of all my observations, I believe that peripheral neuroanatomy
resulting in relatively low visual acuity precludes frequent spontaneous intervention by ringtailed lemurs on behalf of kin and current dominants. All prosimians
lack several anthropoid specializations of the visual system. Even ringtails, among
the most diurnal of prosimians, lack fovea, for example. This and related aspects
of visual anatomy provide ringtailed lemurs less than one-fifth the visual acuity
enjoyed by Papionines, humans, and other Anthropoids (Table IV). As allowed
above, sociocognitive, rather than perceptual, constraints may instead intervene to
preclude matrilineal dominance inheritance for ringtailed lemurs. Also, the various possibilities do not exclude one another. The exciting idea here is that one or
Development and Dominance Among Primates / 165
TABLE 111. Selected Examples of Visual Recognition Errors by Aggressive
Ringtailed Lemurs
24 April 1986-Adult female LY had targeted young immigrant males DI and HI for intense
antiinfanticidal aggression; today, she spotted her son of the same age, AN, approaching from
10-15 m; as often done to DI and HI, she stared, rose, and charged; LY pulled up sharply 1 m
from AN, who had simply stopped walking, and they departed one another peaceably
11 December 1990-Near the boundary between group territories, young adult male GL
spontaneously charged AX, a peer with whom he had been making transfer excursions; GL
stopped suddenly 1 m from his target, sniffed him, and walked away
14 April 1991-Adult female CO saw two pubertal males wrestling in the leaf litter and
charged to attack; immediately after grabbing one of them by the pelage, she dropped him and
walked off, apparently having discovered that he (HC) was her son
8 July 1992-Four months ago, second-ranking adult female CN initiated targeted harassment
of the low-ranking female BU; today, she noticed BU tumble into a bout of wrestling play with
juvenile and adolescent groupmates and interrupted her foraging to rush over to the
interaction, 10 m away; upon arriving, she stood bipedally, bent over the two remaining
players, and paused for 2-3 seconds; CN sniffed first the body of her brother (NT); then, upon
sniffing BU, she immediately grabbed and bit her
more neuroethological limitations seem likely to constrain the development and
evolution of social structure in ringtailed lemurs, with surprisingly far-reaching
ramifications for life-history evolution in these primates.
DEVELOPMENT OF INDIVIDUALS AND THEIR SOCIAL SYSTEMS
Investigation of relationships among classical life-history traits, behavioral
development, and animal social structure has just begun. Focus on these issues can
be expected to increase in research on nonhuman primates, due to our affinities
with these animal taxa and our desire to understand the development of complex
social systems [e.g., Cheney & Seyfarth, 1990; Harcourt & de Waal, 19921. One
purpose of this article has been to emphasize that we can expect to find behavioral
processes-including developmental, perceptual, and cognitive aspects-to be integrated features of the particular life histories under study.
As in all of biology, a principal objective for future research on behavior will be
to identify developmental mechanisms. How do life histories-of individuals and
their groups-self-organize? What causal and functional relationships are responsible for the consistencies in physical, behavioral, and social development observed
across populations and generations? Heretofore, research on development has been
conceived as a different endeavor from that concerned with evolution. Progressively more often today, these two domains of inquiry are properly viewed as
inextricably related and mutually supportive [Buss, 1987; Ho & Fox, 1988; Roth,
1991; Gottlieb, 1992; Salthe, 1993; Hall, 1994). Certainly, to achieve meaningful
understanding of diversity in social systems, normative behavioral development of
individuals must be analyzed in relation to characteristic patterns in physical
development, reproduction, and ecology. Likewise, I argue below, full analysis of
these life-history features must attend to effects of behavioral development and
social systems.
Growth and Adult Social Behavior Shape Behavioral Development
Our overview of physical and behavioral development in two groups of primates introduced substantial evidence of causal and functional relationships be-
166 / Pereira
TABLE IV. Primate Visual Anatomy and Performance*
Prosimians
Galago
Tupaia glis senegalensis
Specialized retinal
structures
Photoreceptors
Maximum density
per 100 mu
Axial eye length (mm)
Mm retina/degree of
visual acuity
Convergence: central
photoreceptors to ganglion
Visual acuity (min of arc)
None
Only cones
21
7
0.09
0.5:l
6.2
Area
centralis
Only rods
88
15
0.19
12:l
4.3
Lemur
catta
Area
centralis
1 cone:
5 rods
20
15
Anthropoids
Saimiri Macaca Homo
sciureus mulatta saviens
Fovea
Fovea
Fovea
Foveal
cones
Foveal
cones
Foveal
cones
60
15
50
20
38
24
0.19
0.18
0.25
0.29
8:1
4.5
1.5:l
0.75
1.5:l
0.75
1.5:l
0.75
*Neuringer et al., 1981; Neuringer, personal communication.
tween these ontogenetic domains. In particular, given marked discontinuities in
development, the riskiest aspects of dominance acquisition were found to be timed
closely with the onset of accelerated growth and maturation. Male and female
Papionines complete their rise in dominance over adult females just before or as
growth spurts and maturation begin. Also, infant ringtailed lemurs establish their
dominance relations just as they begin to help sponsor their own rapid growth. The
next year (or next, depending on nutrition), following dry season suppression of
growth rate, rapid growth is resumed, females sexually mature, and only then do
those living in large or growing groups strive to overturn some adults in dominance, which enables them to begin reproducing without dispersing.
Also supported were our assumption of juvenile risk aversion and prediction
that juveniles seek to maximize their dominance within constraints imposed by
social structure. Adult Papionines intervene systematically in infants’ competitive
interactions before infants themselves seem aware of matrilineal social structure.
But also, infants respond quickly within the system. They readily begin behaving
in a dominant manner toward lowborn peers, and dominance relations are well
established by weaning. Papionine immatures rarely strive to “overachieve” in
dominance, and efforts to dominate much larger or relatively high-ranking group
members are postponed until larger sizes are attained [Datta, 1983a; de Waal,
19931. But also, youngsters instigate fights with older lowborn groupmates when
likely supporters are nearby and solicit assistance over longer distances when
necessary [Pereira, 19921. In the more dimorphic species, young males exploit
females’ apparent disinclinations to oppose them, moving readily into positions of
dominance over female peers and some adult females well before puberty.
Infant ringtailed lemurs strive demonstrably for high dominance among their
birth peers, and probability of survival is likely to be at stake. When necessary,
ringtails stage intense, conspicuous grappling bouts at extremely young ages to
establish their dominance relations. Almost certainly, grappling renders ringtailed infants more vulnerable not only to injury, but also to predators and infanticidal adults [Pereira, 1993~1.The value of size to survival is suggested by basic
photoperiodic regulation of growth effort and the significantly accelerated and
extended growth of late-born and other small infants. Like so many immature
Development and Dominance Among Primates I 167
animals in temperate regions [Boyce, 1988; Pereira, 1993a1, young ringtailed lemurs have a deadline to meet: inevitably, their first long dry season fast approaches. By maximizing their dominance, ringtailed infants promote their
chances of extensive growth and energy storage by mid-autumn [Pereira, 1993b,c;
Pereira & Pond, 19951. Restriction of dominance struggles and high growth effort
to the season of plentiful food minimizes risk of mortality due to malnourishment
for this bottom-ranking class of group members.
Bidirectional Effects in Life-History Evolution
Two major life-history features, one traditional and one nontraditional, provided basic context for our analyses. Each arguably imposes important constraints
on the development and evolution of the social systems discussed. The traditional
feature was pattern of growth. Regardless of why dimorphism varies among papionine taxa, attendent variation in its development appears to influence the manner in which males and females come to interact agonistically, generating basic
variation in social structure. The experiences of juvenile female baboons, for example, multiply confirm for them that males are inappropriate agonistic opponents. Juvenile males, meanwhile, experience that females are easy to dominate,
especially whilst collaborating with other powerful males. These social patterns,
reinforced throughout development, become prominent among adult savanna baboons. By contrast, such experiences are made rare for developing rhesus and
Japanese macaques by the modest relative sizes and growth capacities of pubertal
males in these taxa. Consequently, female rhesus and Japanese macaques maintain relatively great agonistic influence over male behavior, and males in these
taxa continue to orient their coalitionary inclinations as or more heavily into their
relations with females as they do into their relations with males [e.g., Koford,
1963; Packer & Pusey, 19791. Research on populations of varying degrees of dimorphism would provide tests of these ideas.
The species differences in growth pattern and prereproductive experience that
I highlight may act as initial conditions [sensu Salthe, 19851 that promote the
development of additional contrasts in sociobiology. Consider, for example, “special” relationships, or male-female “friendships” in Papionines. Males and females
contribute to and, seemingly, benefit from special relationships differently in different taxa. Male baboons never receive agonistic support from their female
friends, for example, whereas male macaques do [e.g., Chapais, 1983a,b, 1986;
Smuts, 19851. Conversely, male baboons possess a commodity [Noe et al., 19911
that no male rhesus or Japanese macaque does: absolute agonistic power over
females. Related perhaps is that, compared to male baboons, male macaques perform much more grooming of their friends and less often seem favored by them as
mates [Smuts, 1985; Chapais, 1983a,b; Hill, 19901.
The second contextual variable for our analyses was a nontraditional point of
focus in life-history analysis but a classical feature of research on social behavior:
dominance behavior itself. We don’t yet know why some primates practice dominance while others do not [e.g., Pereira & Kappeler, in press]. But the presence or
absence of this mode of agonistic relationship can reasonably be expected to influence life-history evolution, including aspects of growth and social structure. I have
argued, for example, that male baboons subordinate females and females avoid
conflict with males because dominance can mediate access to food in this species.
Accordingly, taxonomic variation in relative size and growth capacity of pubertal
males across taxa might not promote the observed variation in dynamics and
functioning of special relationships (see above) if dyadic dominance was unimportant to papionine monkeys.
168 I Pereira
Ringtailed lemurs well illustrate how classical life-history traits may respond
to aspects of social behavior and how positive feedback can develop in life history
evolution. Earlier, I suggested that birth synchrony evolved in ringtails because
mothers are unable to intervene behaviorally to promote offspring dominance and
because infants compete intensely for dominance around mid-lactation. Birth synchrony, in turn, increases the need for dominance competition among infants,
further enhancing the value of rapid growth. If dominance were unimportant to
the members of this species (e.g., Eulemur fulvus rufus [see Pereira & Kappeler, in
press]), growth and reproduction might exhibit more relaxed and flexible seasonality. Contest competition would be reduced for infants, with peers and adults,
before and during dry seasons.
Ringtailed lemurs provide other examples of complicated relations among lifehistory features. What selection pressure demands that high visual sensitivity
(night vision) be conserved? I suggest annual temperature cycles [see also Morland, 19931. Ringtails spend the summer and early fall not only growing rapidly,
but also growing hair rapidly and accumulating white adipose tissue a t superficial
depots [Pereira & Pond, 1995; Pereira, unpublished data]. During peak summer
temperatures, ringtails extend their characteristic midday “siesta” [Jolly, 19661
from midmorning until late afternoon and spend much of that time panting and
licking their palms and wrists, in efforts to reduce body temperature. Their strategy of coping with environmental seasonality, ironically, includes growing heavy
winter coats during the hottest months. To help with this, much daily activity
during summer and early fall is probably shifted t o the nighttime [see also Jolly,
19661. Ringtails and other gregarious diurnal and semidiurnal lemurs are thought
to have evolved from nocturnal ancestors [Martin, 19901. This inference is supported by an overall life-history response to seasonality that seems better adapted
to a nocturnal life-style. As yet, I suggest, that life-history strategy has obstructed
a complete shift to diurnality and associated social structures, such as dominance
hierarchy maintenance and matrilineal rank inheritance.
CONCLUSIONS
1. Research on growth and behavioral development in papionine monkeys and
ringtailed lemurs has underscored the integrated nature of animal life histories,
from environmental seasonality through sensory, reproductive, and developmental
biology on to social cognition. Understanding the development of primate social
systems will depend on understanding individual development in relation to all
aspects of male and female life histories.
2. Patterns of growth and social structure influence the development of dominance relations in primates. When characteristic discontinuities in growth effort
exist, for example, relatively risky aspects of dominance acquisition occur just
before or as growth spurts begin in papionine monkeys and ringtailed lemurs.
Also, female papionines rarely try to dominate females from families higher ranking than their own. See also conclusions 3 and 4.
3. Patterns of development can influence reproductive biology. Reproductive
synchrony, for example, probably evolved in ringtailed lemurs because (1)females
are unable to intervene to promote offspring dominance, (2) infants grow rapidly in
part to attain the large size that conveys high dominance, which continues to
enhance growth rate and probability of survival, and (3) birth synchrony precludes
an insurmountable initial advantage for any female’s infants.
4. Patterns of development influence social structure. Across multimale papionine taxa, for example, increases in pubertal size andlor growth capacity of males
relative to females are associated with decreases in female inclination to t r y and
Development and Dominance Among Primates / 169
dominate males, regardless of age class. Male and female perceptions of males and
females as potential partners and opponents in social conflicts seem to be reinforced
bidirectionally across the life span and relate importantly to known differences in
social structure.
5. Aspects of growth, reproduction, and social structure in primates are
probably influenced by characteristic patterns of dyadic social behavior. The
phenomena cited in conclusions 3 and 4, for example, may depend importantly
on the characteristic expression of dominance behavior in these monkeys and
lemurs.
6. In ringtailed lemurs, an integrated set of physiological responses to photoperiodic cycling corroborates the suspected origin of these primates among nocturnal taxa.
7. Certain responses to photoperiod, such as fat storage and hair growth in
summer and fall, may require ringtailed lemurs to retain good nocturnal vision,
and consequent limitation of visual acuity may constrain social structure (e.g., by
precluding maternal rank inheritance).
ACKNOWLEDGMENTS
I thank the Director, Dr. K. Glander, for permission to research at the DUPC,
and Dr. A. Jolly, Dr. H. Crowley, and especially Mr. J . de Heaulme for both
permitting and facilitating my research a t the Berenty Reserve. L. Martin, F.
Kaestle, J. Opperman, A. Wang, L. Yow, L. Santini, C. Dina, and J . Schackleford
assisted with behavioral observations, and K. Alford-Madden, D. Brewer, S. Cavigelli, P. Kappeler, L. Martin, T. Mendelson, F. Stewart, and L. Vick assisted in
obtaining body weight data from DUPC ringtailed lemurs. To many researchers I
am deeply grateful for permissions to present unpublished data: on juvenile dominance relations, M. van Noordwijk and A. Baker; on growth trajectories, C. van
Schaik; and on visual anatomies and acuities, M. Neuringer. D. Hill, S. Perloe, D.
Sprague, and L. Wolfe advised me on the intervention behavior of adult male
macaques, and A. Jolly and N. Koyama provided historical information on ringtailed social groups, especially T Group, at Berenty. Data on infant grappling
between 1981 and 1983 were documented by L. Taylor [1986]. My research and
writing were supported by the National Institute of Child Health and Human
Development (R29-HD232431,the Chicago Zoological Society, the Duke University
Primate Center, and Terri-Jean Pyer. My deepest gratitude goes to T.-J. Pyer,
whose unflagging support has generated most of the time I have needed to conduct
my research. This is DUPC publication 610.
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