The role of play in social organization: Comparative observations on squirrel monkeys (Saimiri)

Various functional theories of play stress that social play is essential for the practice and learning of sex roles, dominance relationships, troop culture, integration of individuals into the troop structure, the control of aggression, etc. Data on squirrel monkeys (Saimiri) in natural environments indicate that social interaction and troop integration can develop in various manners in the absence of social play.Comparative observations were made on squirrel monkeys in a seminatural environment in Florida and 43 natural environments in Panama, Colombia, Peru, and Brazil. There was a broad range of variance in the data on ecology, troop size, troop cohesiveness, average individual distances, frequency of play, etc. In some environments, individuals in the infant and juvenile age classes engaged in social play for approximately 1.5 to 3 hours a day. However, in one environment, not a single incidence of social play occurred during 261 hours of close range observation. The troops in which no play occurred were very cohesive (i.e., they seldom fragmented), and the animals traveled at close individual distances. Agonistic interactions were not uncontrolled. Copulations were observed; and 85 percent of the adult females were accompanied by infants, which indicates a normal rate of reproductive success for the species.Data are presented on friendly, aggressive, sexual, and spacing behavior in squirrel monkeys. These data indicate that (1) social play is not necessary for the development and/or learning of an adaptive modicum of social interaction patterns and troop cohesion, but (2) the opportunity to play provides learning experiences in which young animals can develop more complex, varied social interaction patterns and stronger habits for engaging in frequent social exchanges.     

Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: A comparison with captive pairs

The general course of mother-infant relationships among free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago is remarkably similar both qualitatively and quantitatively to that observed in the socially living captive colony at the MRC Unit at Madingley, England. Nevertheless, small but consistent differences appear to be due to differences between mothers in the two environments rather than differences between infants. Captive mothers may be described as more protective and less encouraging of early independence in their infants than free-ranging mothers. Moreover, captive pairs have become more like free-ranging pairs over the years, perhaps as captive mothers have been allowed to raise their infants in the presence of kin. A unitary concept of environmental complexity is not useful in accounting for the results.     

Nature Needs Nurture: The Interaction of Hormonal and Social Influences on the Development of Behavioral Sex Differences in Rhesus Monkeys

Thirty years of research on early social and hormonal environments and their relationship to the expression of behavioral sex differences in rhesus monkeys are reviewed. These studies demonstrate that whether aggressive and submissive behaviors are sexually dimorphic depends primarily on the social and not the hormonal environment. Early rearing environments without mothers or allowing brief periods of peer interaction produced higher levels of male aggression and female submission. Presenting behavior was expressed more by females than males in environments with high male aggressivity and female submissiveness. No sex differences in presenting occurred in low aggressivity environments, unless monkeys were reared isosexually, when males presented more than females. Rough and tumble play and foot-clasp mounting were consistently exhibited more by males than females across all rearing environments studied, but rearing environment affected the degree of the sex difference. When reared isosexually males displayed less, and females more, foot-clasp mounting than when heterosexually reared. No social environment increased the low frequency of female rough and tumble play. Suppressing neonatal androgen in males did not effect any sexually dimorphic behavior. Prenatal androgen administration to genetic females masculinized many aspects of their juvenile behavior, consistently increasing rough and tumble play and foot-clasp mounting across different social environments. Thus the sexually dimorphic behaviors which showed the smallest variability across social contexts were the most profoundly affected by the prenatal hormonal environment. These studies demonstrate that the expression of consistent juvenile behavioral sex differences results from hormonally induced predispositions to engage in specific patterns of juvenile behavior whose expression is shaped by the specific social environment experienced by the developing monkey.     

Physiological effects of dominance hierarchies: laboratory artefacts or natural phenomena?

Studies of fish behaviour have demonstrated the existence of social interactions that result in dominance hierarchies. In environments in which resources, such as food, shelter and mates, are limited, social competition results in some fish becoming dominant and occupying the most profitable positions. This behaviour has been observed in natural environments and also in many laboratory‐based experiments. When two fish have been confined in a small tank, one of them usually has exhibited behaviour that suggests it is dominant over the other submissive animal. Physiological consequences of social interaction can be seen in both dominants and subordinates but are more extreme in the subordinate. However, this scenario is without doubt an artificial situation. Fewer experiments have been conducted using laboratory experiments that are more socially and physically complex than those experienced by dyads in tanks. In simple fluvial tanks, through which water is recirculated, the physiological responses of fish to social competition have generally been qualitatively similar to those recorded among dyads. However, when environmental disturbances, complex resource distributions, increase in water flushing, presence of predators and competing species of fish have been included in experimen‐tal designs, there have been fewer, diminished or no physiological dierences between dominant and subordinate fish. There have been very few studies of physiology in relation to dominance in natural habitats, and those that have been conducted suggest that under some circumstances hierarchies may cause less intense physiological responses than have been suggested based on results of laboratory studies in simple environments. Possible reasons for these variations are discussed. The need is identified for a well structured experimental approach to the investi‐gation of the causes and consequences of hierarchies if the ecology of wild fish is to be modelled eectively based on physiological processes. It is also suggested that the further development and application of techniques for monitoring physiologies of fish in the wild is important.     

Stone banging by wild capuchin monkeys: an unusual auditory display

Primates often react to possible predators by using intimidation displays, although the occurrence of these displays is dependent on the risk of predation. Functional explanations for these kinds of displays range from sexual selection to predator deterrence. The ability to respond to different predators can be socially acquired, and social traditions could explain population differences in response to the same potential predator. Here I report wild groups of Cebus apella libidinosus banging stones to produce sound in a remarkable aggressive display. I observed this display in 6 wild groups and I suggest its primary function is a predator-deterrent behaviour. Although banging objects is an innate behaviour in capuchin monkeys, in all wild groups observed so far it has been observed only in a foraging context. Stone banging is a novel behavioural variant that is most likely learned socially. The absence of this display in other populations of capuchins, which have access to stones, suggests that stone banging could be a social tradition in the population studied.     

Reproductive Behavior in the Rhesus Monkey: Social and Endocrine Variables

SYNOPSIS. Social groups of rhesus monkeys (Macaca mulatto) livingin outdoor environments exhibit a distinct seasonal mating patternand female rhesus are observed to be sexually receptive fordiscrete periods averaging about 9 days duration. In the laboratoryenvironment mating occurs throughout the year and, in the pairtest, female rhesus are observedto be sexually receptive throughall phases of a menstrual cycle, with a periovulatory peak incopulatorybehavior. The apparent conflict between results from field andlaboratory studies has been difficult to resolve because ofmethodological limitations inherent in each study environment.Studies conducted on social groups of rhesus monkeys housedin outdoor compounds, an environment in which the species typicalseasonal mating pattern is preserved and which allowsfor concomitantmeasurement of behavioral and hormonal variables, provided informationabout the covariance between female sexual behavior and ovariancycles. Female copulations were observed only in associationwith ovulatory cycles, and were limited to the follicular andperi-ovulatory phases of such cycles, demonstrating that copulatorybehavior in female rhesus monkeys is strongly influenced bycyclic hormonal variables. The studies also revealed that femalestend to conceive on the first ovulatory cycle of the season,that there was no synchrony of cycles among the females, andthat the best predictor of the timing of ovulation in a particularfemale is reproductive outcome in the previous year.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Reproductive skew among males in a female-dominated mammalian society

The purpose of this study was to document patterns of reproductiveskew among male spotted hyenas (Crocuta crocuta), a speciesin which many normal mammalian sex roles are reversed. We usedpaternity determined from 12 microsatellite markers togetherwith demographic and behavioral data collected over 10 yearsfrom a free-living population to document relationships among reproductive success (RS), social rank, and dispersal statusof male hyenas. Our data suggest that dispersal status andlength of residence are the strongest determinants of RS. Natalmales comprise over 20% of the adult male population, yet theysire only 3% of cubs, whereas immigrants sire 97%. This reproductiveadvantage to immigrants accrues despite the fact that immigrants are socially subordinate to all adult natal males, and it providesa compelling ultimate explanation for primary dispersal inthis species. High-ranking immigrants do not monopolize reproduction,and tenure accounts for more of the variance in male reproductivesuccess than does social rank. Immigrant male hyenas rarelyfight among themselves, so combat between rivals may be a relativelyineffectual mode of sexual selection in this species. Instead,female choice of mates appears to play an important role in determining patterns of paternity in Crocuta. Our data supporta "limited control" model of reproductive skew in this species,in which female choice may play a more important role in limitingcontrol by dominant males than do power struggles among males.     

A comparison of cell-mediated immune responses in rhesus macaques housed singly, in pairs, or in groups

A variety of psychosocial factors have been shown to influence immunological responses in laboratory primates. The present investigation examined the effects of social housing condition on cell-mediated immune responses, comparing rhesus macaques (Macaca mulatta) in three housing conditions (single, pair, and group). Subjects included 12 adults of both sexes in each housing condition (N=36). Multiple blood samples (0, 4, 8, and 12 months) were collected for immunological analyses, including lymphocyte subsets, lymphocyte proliferation to pathogens and nonspecific mitogens, natural killer cell activity, and cytokine production. CD4(+) to CD8(+) ratios differed significantly across housing conditions and singly caged subjects had significantly lower CD4(+)/CD8(+) after the 4-month timepoint than did socially housed (pair and group) subjects. CD4(+) to CD8(+) ratios were positively correlated within subjects, suggesting a trait-like aspect to this parameter. Lymphocyte proliferation responses to all four gastrointestinal pathogens differed across housing conditions (at least at the 0.08 level), as did proliferation responses to StaphA, and the production of cytokines (IFN-gamma, IL-2, and IL-10). Proliferation responses of singly caged monkeys did not differ from socially housed monkeys and the highest levels of both IFN-gamma and IL-10 were produced by group housed subjects. The data demonstrate that social housing condition affects immune responses. While not unidirectional, these effects generally suggest enhanced immune responses for socially housed animals. Since rhesus monkeys live socially in nature, and the immune responses of singly housed animals differed from those housed socially, there is considerable motivation and justification for suggesting that the use of singly housed rhesus macaques may complicate interpretations of normal immunological responses. This may have important implications for the management, treatment, and selection of primate subjects for immunological studies.     

Social transmission of maladaptive information in the guppy

Many animals are capable of learning from others, a processreferred to as social learning. There is little doubt that acapacity for social learning is an adaptation and that it typicallyresults in adaptive behavior. What is less clear is whetherthere are circumstances under which social learning can resultin the transmission of outdated, inappropriate, or maladaptiveinformation. Here we report an experimental study that investigatedthe social learning and transmission of maladaptive foraginginformation through small social groups of guppies, Poeciliareticulata. This experiment used a transmission chain designin which fish in small founder groups were trained to take eitheran energetically costly circuitous route to a feeder or a lesscostly short route, with trained founder members gradually replacedby untrained conspecifics. Three days after all the foundershad been removed, the behavioral traditions of groups of untrainedfish were still strongly influenced by their founder's behavior.Moreover, the rate at which untrained subjects that shoaledwith founder conspecifics trained to take the long route learnedto take the short route was significantly slower than for fishforaging alone. The results provide unequivocal evidence thatmaladaptive information can be socially transmitted throughanimal populations and imply that socially learned informationcan inhibit learning of the optimal behavior pattern.     

The genetic consequences of primate social organization: a review of macaques,baboons and vervet monkeys

Primates, as long-lived, iteroparous, socially complex mammals, offer the opportunity to assess the effects of behavior and demography on genetic structure. Because it is difficult to obtain tissue samples from wild primate populations, research in this area has largely been confined to terrestrial and semi-terrestrial old world monkeys (e.g., rhesus and Japanese macaques, vervets and several subspecies of baboons). However, these species display a multi-male, multi-female social structure commonly found in many other primate and non-primate mammals. Electrophoretic analyses of blood proteins from individually recognized and/or marked wild Himalayan rhesus monkeys, themselves the subject of long-term behavioral and demographic research, have begun to reveal the genetic consequences of such phenomena as social group fission, malelimited dispersion, non-consanguineous mating patterns, and agonistically defined male dominance.Specifically, rhesus social groups, consisting primarily of clusters of maternal relatives, appear to be nonrandom samples of a population's genotypes and genes. The genetic effects of social group fission are highly dependent on each group's size, demographic structure, and average degree of relatedness. In all cases fission contributes to the degree of intergroup genetic differentiation. Male-limited dispersion appears both to retard genetic differentiation between social groups and to lead to mating patterns that result in an avoidance of consanguinity. Groups, therefore, appear to be genetically outbred.Comparing these results with studies of other free-ranging or wild cercopithecines allows several generalizations: (a) genetic variation seems to be evenly distributed throughout each local population of multi-male social groups; (b) social groups, however, because they contain clusters of relatives, are distinctive in their specific frequencies of genes; (c) the degree of genetic differentiation between a population's social groups, because of the effects of social group fission and non-deterministic forms of male dispersal, is somewhat greater than expected on the basis of migration rates alone; and (d) the asymmetrical pattern of dispersion with respect to sex effectively precludes inbreeding in any one social group or the population as a whole. These observations have important implications for understanding the unusually rapid rates of evolution among the primates.     

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.     

The Effects of Nitrogen on Five Varieties of Antirrhinum majus

Five F₁ hybrid varieties of Antirrhinum majus were grown infive levels of nitrogen through a period of long days. Significant differences were found between the varieties forall 14 characters assessed and all but two of the charactersvaried significantly with nitrogen levels. Some of the charactersshowed simple responses to increasing nitrogen but seven showedsignificant variety-environment interactions, indicating thatthe response of a given variety relative to the others dependedon which environment it was grown in. Where possible, theseinteractions have been analysed using the linear regressiontechnique to examine the relative degree of response of thevarieties to the range of nitrogen environments.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Vocal similarities and social bonds in Campbell's monkey (Cercopithecus campbelli)

This study examined variations of social call structures in female Campbell's monkeys. The comparison of frequency modulations using a similarity index revealed that each individual presented one to three variants. Some variants were shared by two to several individuals, often associated with play. On the contrary, vocal divergence was observed in a socially isolated animal and a negative correlation appeared between similarity index and the frequency of avoidance. This preliminary study gives the first evidence of variant sharing between group members in primates.     

The ontogeny of play in feral olive baboons (Papio anubis)

Behaviours that always appear playful (play markers) are distinguished from behaviours that appear playful in some contexts, but not others (context-dependent play components). Age changes in the frequency of performance of both kinds of playful behaviours are described, as are age changes in the frequency with which context-dependent play components accompany play markers in baboon social interactions. Some quantitative properties of social interactions containing and lacking play markers are compared. Interactions with play markers last longer and have a higher rate of change of constituent behaviours than interactions without. Animals are also more persistent in the face of changes in their partner's behaviour in interactions with play markers. It is suggested that an attempt to produce a definition of play is not a useful enterprise, but that it is important to investigate causal mechanisms underlying behaviours that appear playful to human observers, and to clarify the relationships among those mechanisms. Data are presented suggesting that at least two sets of mechanisms, not totally separate, underly the performance of baboon social play. Functions of the behaviours controlled by these mechanisms are discussed.     

Cellular Neuronal Control of Molluscan Heart

Bivalve and gastropod molluscs undergo large changes in externalenvironmental conditions, as well as in internal state. Cardiacresponses to these changing conditions have been recorded ina variety of species. There is a general tendency for heartrate, and presumably cardiac output, to increase in responseto situations that would increase the load on respiratory andexcretory systems. Changes in molluscan heart function in manycases appear not to be mediated directly by cardiac nerves,but rather by such indirect mechanisms as changes in blood constituentsor mechanical, hemodynamic effects on heart muscle. Three typesof cardiac response in Aplysia have been shown to be mediated,at least in part, by the heart regulator nerves. The neural circuits that regulate heart rate in Aplysia andin Helix have been partially described in cellular detail. InMercenaria, Aplysia and other molluscan species there is evidencethat cyclic adenosine monophosphate has a role in mediatingthe excitatory effects of serotonin on heart muscle. There appearsto be, in fact, a general tendency in the Aplysia nervous systemfor neurons that exert tonic, modulatory effects within neuralnetworks that control a variety of behaviors to use serotoninfor a transmitter. In each case there is evidence to suggestthat changes in cyclic adenosine monophosphate levels may mediatesome of the modulatory effects of serotonin.     

Social behavior of captive,group-living Orangutans

The behavior of orang-utans (Pongo pygmaeus)was observed in two captive groups (one adult group, one juvenile group). Activity profiles,animal interactions, and compartmental spatial use for both adult-group and juvenile-group individuals were recorded over a 9-month period. Behavioral repertoires for both groups included large amounts of social activity. Equivalent amounts of social activity were found for each group. The social behavior of juvenile animals involved more active behavior such as play. The social behavior of the adult animals was more subtle, involving social monitoring and allogrooming. These results indicate that orangutans, at least when group-living in captivity, exhibit the potential to display social behavior which is apparently of greater frequency and complexity than that which has been observed in the wild. These findings suggest that the solitary behavior of wild orangutans is not a necessary characteristic of orangutan behavior. Under different environmental conditions orangutans appear to readily adapt socially, and, like other nonhuman primates,they have the capacity to exhibit complex and subtle social behavior. This report is based on part of a senior thesis submitted by Sara D. Edwards     

Dominance rank predicts social network position across developmental stages in rhesus monkeys

Social network analysis is increasingly common in studying complex interactions among individuals. Across a range of primates, high-ranking adults are generally more socially connected, which results in better fitness outcomes. However, it still remains unclear whether this relationship between social network position and dominance rank emerges in infancy and whether, in species with a social transmission of dominance rank, social network positions are driven by the presence of the mother. To fill this gap, we first explored whether dominance ranks were related to social network position, measured via eigenvector centrality, in infants, juveniles, and adults in a troop of semi-free-ranging rhesus macaques (Macaca mulatta). We then examined relationships between dominance rank and eigenvector centrality in a peer-only group of yearlings who were reared with their mothers in either a rich, socially complex environment of multigenerational (MG) kin support or a unigenerational group of mothers and their infants from birth through 8 months. In Experiment 1, we found that mother's network position predicted offspring network position and that dominants across all age categories were more central in affiliative networks (social contact, social grooming, and social play). Experiment 2 showed that high-ranking yearlings in a peer-only group were more central only in the social contact network. Moreover, yearlings reared in a socially complex environment of MG kin support were more central. Our findings suggest that the relationship between dominance rank and social network position begins early in life, and that complex early social environments can promote later social competency. Our data add to the growing body of evidence that the presence/absence of the mother and kin influence how dominance rank affects social network position. These findings have important implications for the role of caregivers in the social status of developing primates, which ultimately ties to health and fitness outcomes.