Aggression and social support predict long‐term cortisol levels in captive tufted capuchin monkeys (Cebus [Sapajus] apella)

Many nonhuman primates live in complex social groups in which they regularly encounter both social stressors such as aggression and social support such as that provided by long‐term affiliative relationships. Repeated exposure to social stressors may result in chronically elevated cortisol levels that can have deleterious physical effects such as impaired immune function, cardiovascular disease, and reduced brain function. In contrast, affiliative social relationships may act as a buffer, dampening the release of cortisol in response to acute and chronic stressors. Understanding how social stressors and social support predict cortisol levels is therefore essential to understanding how social situations relate to health and welfare. We studied this relationship in 16 socially housed captive brown capuchin monkeys (Cebus [Sapajus] apella) by comparing long‐term hair cortisol levels with behavioral measures of social stress (dominance rank, rank certainty, and amount of aggression received) and social support (amount of affiliation and centrality in the affiliative social network of the group). Dominance rank, rank certainty, amount of affiliation, and age were not significant predictors of long‐term cortisol levels in this population. Instead, long‐term cortisol levels were positively related to the amount of aggression received and negatively related to centrality in the affiliative social network of the group. This pattern may be attributed to the species’ socially tolerant dominance system and to the availability of social support across the dominance hierarchy.     

White-faced capuchin monkeys show triadic awareness in their choice of allies

The social intelligence hypothesis, which holds that social challenges have selected for increased intelligence and social skills, has been supported by evidence that, in catarrhine primates, individuals know about the characteristics of groupmates' social relationships. Evidence for such ‘triadic awareness’ has not been sought for platyrrhine primates, although two platyrrhine genera, capuchins, Cebus, and squirrel monkeys, Saimiri, are among the most highly encephalized primates. We examined patterns of coalitionary recruitment in wild white-faced capuchins, C. capucinus. Analyses have shown that more dominant individuals are more likely to join aggressive coalitions than low-rankers, and that individuals preferentially support those with whom they have stronger affiliative relationships. Data from 110 fights, analysed using simulation techniques that produced distributions of results expected under null hypotheses, revealed that contestants preferentially solicited prospective coalition partners that (1) were dominant to their opponents, and (2) had better social relationships (higher ratios of affiliative/cooperative interactions to agonistic interactions) with themselves than with their opponents. Further analyses showed that soliciting dominant partners could be explained by either of two simpler rules, ‘Solicit an ally that outranks yourself’ or ‘Solicit the highest-ranking available individual’. However, soliciting partners with better social relationships appears to indicate triadic awareness, because subjects did not preferentially solicit the nearby individual with whom they shared the highest-quality social relationship. Effects of relative relationship quality on coalition solicitation decisions were independent of effects of dominance rank.     

Squirrel monkeys (Saimiri) in natural habitats in Panama,Colombia, Brazil,and Peru

Troops ofSaimiri (squirrel monkeys) were observed in 31 locations in natural habitats in Panama, Colombia, Brazil, and Peru. Troop size varied from 10 to 35 animals in Panama and Colombia and from 120 to 300 or more in the unaltered rainforests of Amazonia. Troop size correlated with forest size in all areas.Saimiri associated withCebus (capuchin monkeys) in several areas.Saimiri troops showed different responses to man, fear and flight or neutral responses or curiosity; and these correlated with local environmental conditions. Social behavior varied significantly between the large and small troops. Social interactions were much more frequent and individual distances were much smaller in the large troops than in the small troops. Several factors that may relate to these differences in sociability are discussed in light of data from this and other studies.     

Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina)

The tendency in primates for former antagonists to approach and affiliate following aggression has been termed reconciliation because the response is thought to resolve social conflicts produced by aggression. In primate societies, however, an aggressive interaction between two individuals often spreads to include other group members, especially the kin of the combatants. If post conflict affiliation resolves aggressive conflicts in a group, then affiliative increases might occur between combatants and the kin of their opponents following aggression as well as between former opponents. This hypothesis was tested in a captive group of 39 pigtail macaques (Macaca nemestrina) by comparing affiliative response frequencies of combatants during the 5 minute period following aggression to affiliative response frequencies during 5 minute baseline periods not preceded by aggressive activity. Following aggression, affiliation rates increased between combatants and their opponents, aggressors and the kin of their opponents, and aggressors and their own kin. Additional analyses showed that aggression among kin was reconciled more often than aggression among nonkin. Recipients of aggression reconciled with their attackers more often than aggressors reconciled with their victims. Animals with similar dominance ranks reconciled proportionately more often than those with large rank disparities and aggressive infractions of a calculated dominance hierarchy were reconciled more often than attacks consistent with the hierarchy. Results suggest that both dyadic and triadic reconciliations occur in M. nemestrina and that compared to other primate species M. nemestrina exhibit a moderate-to-high conciliatory tendency.     

Reconciliation following aggression in patas monkeys,Erythrocebus patas

Following intra-group aggression, obvious conciliatory displays are absent from the behavioural repertoire of patas monkeys, Erythrocebus patas, while many other Old World primate species show special reconciliation gestures. When 10-min focal-animal samples that began after spontaneous aggression were compared with matched-control samples, captive adult female patas followed up on aggressive interactions, interacting sooner and more often with former opponents during post-conflict observations than during matched-control observations. Almost one-third of post-conflict observations included affiliative behaviour between former opponents, which is termed reconciliation. Matrilineally related opponents were more likely to reconcile with one another than were unrelated animals. No effect of the dominance hierarchy on tendency to reconcile was found. Thus, patas monkeys showed general patterns in post-conflict behaviour that were similar to those seen in other primates previously investigated.     

Interspecific Infanticide and Infant‐Directed Aggression by Spider Monkeys (Ateles hybridus) in a Fragmented Forest in Colombia

Interspecific aggression amongst nonhuman primates is rarely observed and has been mostly related to scenarios of resource competition. Interspecific infanticide is even rarer, and both the ultimate and proximate socio‐ecological factors explaining this behavior are still unclear. We report two cases of interspecific infanticide and five cases of interspecific infant‐directed aggression occurring in a well‐habituated primate community living in a fragmented landscape in Colombia. All cases were initiated by male brown spider monkeys (Ateles hybridus) and were directed toward infants of either red howler monkeys (Alouatta seniculus: n = 6 cases) or white‐fronted capuchins (Cebus albifrons: n = 1 case). One individual, a subadult spider monkey male, was involved in all but one case of interspecific infanticide or aggression. Other adult spider monkeys participated in interspecific aggression that did not escalate into potentially lethal encounters. We suggest that competition for food resources and space in a primate community living in high population densities and restricted to a forest fragment of ca. 65 ha might partly be driving the observed patterns of interspecific aggression. On the other hand, the fact that all but one case of interspecific infanticide and aggression involved the only subadult male spider monkey suggests this behavior might either be pathological or constitute a particular case of redirected aggression. Even if the underlying principles behind interspecific aggression and infanticide are poorly understood, they represent an important factor influencing the demographic trends of the primate community at this study site. Am. J. Primatol. 74:990‐997, 2012. © 2012 Wiley Periodicals, Inc.     

Social organization of a stable natal group of captive Guyanese squirrel monkeys (<Emphasis Type="Italic">Saimiri sciureus sciureus</Emphasis>)

Socioecological models suggest competition for food, foraging efficiency, predation, infanticide risk, and the costs of dispersal regulate primate social structure and organization. Wild populations of squirrel monkeys (Saimiri spp.) appear to conform to the predictions of the predation/competition socioecological model (Sterck et al. in Behav Ecol Sociobiol 41:291–309, 1997) and the dispersal/foraging efficiency model (Isbell in Kinship and behavior in primates. Oxford University, New York, pp 71–108, 2004). However, squirrel monkeys in captivity are reported to maintain patterns of social behavior observed in their wild conspecifics despite different food distribution, predation risk, and dispersal options. This behavioral similarity suggests squirrel monkeys’ social behavior has limited flexibility to respond to environmental changes. In this study, we experimentally evaluated the flexibility of social behavior within a captive group of S. sciureus. First, we determined whether dominance and affiliative relationships observed under normal laboratory conditions (with abundant, widely distributed, food; no dispersal option; and no predators) better matched published reports of relationships among wild conspecifics or the predictions of the predation/competition model. Second, we made preferred food items defensible to determine whether dominance interactions would become more frequent and linear, as predicted by the model. The model correctly predicted rates of dominance behavior in both conditions and a linear hierarchy in the defensible food condition but did not predict the consistent affiliative relationships and linear dominance hierarchy observed in normal lab conditions. Although hierarchies were linear and male dominant, manipulating food distribution changed the dominant individual within each sex. Our findings suggest interaction rates adapt more rapidly than social structure to environmental changes in Saimiri and recommend caution in interpreting tests of socioecological models.     

Competition and Facilitation in the Capuchin–Squirrel Monkey Relationship

In Guyana, the range of the brown capuchin, Cebus apella, meets the range of its congener, the wedge‐capped capuchin, C. olivaceus, with the two species exhibiting a mutually exclusive patchy distribution. Squirrel monkeys, Saimiri sciureus, and C. apella form ubiquitous interspecific associations, but the reason remains debatable. With a large biogeographic field study, we tested the degree to which the distribution and abundance of Cebus and S. sciureus is determined by habitat type, fruit availability, and geography (i.e., determinants of the fundamental niche) relative to interspecific interactions, such as competition and facilitation (i.e., the realized niche). We used the competition between the two capuchin monkeys as a natural experiment that subjected S. sciureus to C. apella and C. olivaceus ‘treatments’. Using spatial regression models and principal components analysis, we found that S. sciureus was associated with seasonally flooded forests, and was correlated with fruit abundance and diversity (fundamental niche), but was also correlated with C. apella density even when accounting for habitat and fruit availability (realized niche). Saimiri sciureus density was unrelated to C. olivaceus density. Cebus apella was associated with a variety of forest types, but particularly included disturbed and edge habitats such as logged forests, seasonally flooded forests, and upland savanna, in addition to mature forest. Cebus apella was also positively correlated with S. sciureus density and negatively correlated with the density of C. olivaceus. In contrast, C. olivaceus avoided riparian areas and was associated with mixed‐height forests on sloped mountainous terrain. In sum, interspecific interactions such as competition between species of Cebus and facilitation between C. apella and S. sciureus were as important as habitat and fruit availability in determining the distribution and abundance of these primates.     

Affiliative and Aggressive Behavior in a Group of Female Somali Wild Ass (Equus africanus somalicus)

We observed a group of three young female Somali wild asses to develop an ethogram of social behavior in the first phase of a longer term study of social, sexual, and maternal/infant behavior. The most unexpected finding was the frequency and extent of aggressive interactions, which included Charge, Drive, Neck Wrestle, Head Butt, and Body Slam, behaviors previously reported only for males of other equid species. The overall frequency of aggressive behavior was higher than that of affiliative behavior (84±16.5 vs. 32±5.5, P=0.03), yet no injuries occurred. The dyadic directionality of aggressive behavior suggested a dominance hierarchy, a feature not previously reported for either wild ass or domestic donkeys. The aggression observed may be an accurate representation of the behavior of this species, or their relatively young ages, or their recent transfer from their natal group through quarantine and into a new enclosure may have heightened agonistic tendencies. Further studies will determine whether with time their aggressive behavior becomes more intense or dissipates with maturity. Zoo Biol 31:87;–97, 2012. © 2011 Wiley Periodicals, Inc.     

A new fossil cebine from hispaniola

An incomplete mandibular fragment of a cebine monkey from an early Holocene Haitian cave deposit adds to the small but growing list of fossil Antillean primates. The jaw is of the correct size to belong to the same taxon as the partial maxilla of “Saimiri” bernensis from the Dominican Republic. Both finds probably represent a single species whose proximate ancestry lay closer to Cebus than to Saimiri, although more evidence will be required to substantiate this. No close relationship of the Hispaniolan fossils to the Jamaican platyrrhine Xenothrix is indicated. How monkeys managed to penetrate the West Indies is a biogeographical puzzle of the first order. Geographical vicariance events, island-hopping, and purposeful or inadvertent introduction by humans seem rather implausible devices. On the whole, long-distance, over-water rafting from the Americas remains the most likely mechanism for past land vertebrate immigration into the Caribbean.     

Intra and Interspecific Variation in Cranial Morphology on the Southernmost Distributed Cebus (Platyrrhini,Primates) Species

Capuchin monkeys (Cebus) are one of the genera with the widest distribution among Neotropical primates (New World Monkeys, Platyrrhini), accompanied by an elevated genetic, phenotypic, behavioral, morphological, and ecological diversity, both at the interspecific and population levels. Despite being one of the most studied primate genera, this high diversity has led to a particularly complex and controversial taxonomy. In this contribution, we explored the patterns of skull size and shape variation among the southernmost distributed populations of Cebus using three-dimensional geometric morphometric techniques. Results showed a marked morphological differentiation (in size and shape) between previously recognized species (C. nigritus and southern C. libidinosus), and also among C. libidinosus populations, which were quantitatively related with the geographic distance between them. This pattern supports a differentiation between the northwestern Argentina and southern Bolivia and Paraguay forms. Other taxonomic implications are also discussed.     

Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory‐housed primates than day of week

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory‐housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory‐housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on “bright” nights than “dark” nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft‐cited weekend effect hypothesis.     

Milk composition of captive tufted capuchins (Cebus apella)

Little is known about the milk composition of nonhuman primates, and it has never been examined in capuchin monkeys (genus Cebus). This article reports on the macronutrient milk composition (fat, crude protein (CP), lactose, dry matter (DM), and total gross energy (GE)) of captive housed tufted capuchins (Cebus apella) (n=8). C. apella milk averaged 5.22% fat, 2.40% CP, 6.94% lactose, 16.48% DM, and 0.89 kcal/g. Fat was the most variable macronutrient and was significantly higher in samples collected after 2 months of lactation. To explore the adaptive significance of C. apella milk composition, results were compared with data on milk composition from a closely related cebid, Saimiri boliviensis boliviensis, and another large‐brained anthropoid, Homo sapiens. C. apella milk was only significantly different from Saimiri milk in CP and the proportion of energy from CP. Compared with human milk, C. apella milk was lower in lactose but higher in fat, CP, DM, GE, and the proportion of energy from CP. Results from this small dataset suggest that among anthropoid primates, the macronutrient composition of milk is influenced by phylogeny, may vary relative to infant growth rates, but may not be related in any direct way to relative brain size. Am. J. Primatol. 72:81–86, 2010. © 2009 Wiley‐Liss, Inc.     

Postconflict Behavior of Spectacled Leaf Monkeys (Trachypithecus obscurus). II. Contact with Third Parties

We studied the postconflict interactions with group members other than the former opponent in two groups of spectacled leaf monkeys. We found no evidence of redirection of aggression towards other group members. Victims and aggressors sought affiliative contacts with uninvolved third parties. There was no evidence for consolation—affiliative contact initiated by an uninvolved third party, directed towards victims of aggression—in either group when all affiliative behaviors were considered. However, embracing was a characteristic first-contact interaction between individuals involved in aggression and third parties. This finding mirrors the results concerning reconciliation in spectacled leaf monkeys. Accordingly, embracing may be a true consolatory behavior in this species. When contacts with third parties occurred before or in the absence of reconciliation, the timing of such contacts fell within the time window during which reconciliation normally occurs. These contacts also resulted in affiliation levels twice that of baseline levels, supporting the idea that these contacts may function as a form of substitute reconciliation. We discuss these results in light of recent theories concerning postconflict behavior in primates.     

When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini)

Background

How are morphological evolution and developmental changes related? This rather old and intriguing question had a substantial boost after the 70s within the framework of heterochrony (changes in rates or timing of development) and nowadays has the potential to make another major leap forward through the combination of approaches: molecular biology, developmental experimentation, comparative systematic studies, geometric morphometrics and quantitative genetics. Here I take an integrated approach combining life-history comparative analyses, classical and geometric morphometrics applied to ontogenetic series to understand changes in size and shape which happen during the evolution of two New World Monkeys (NWM) sister genera.

Results

Cebus and Saimiri share the same basic allometric patterns in skull traits, a result robust to sexual and ontogenetic variation. If adults of both genera are compared in the same scale (discounting size differences) most differences are small and not statistically significant. These results are consistent using both approaches, classical and geometric Morphometrics. Cebus is a genus characterized by a number of peramorphic traits (adult-like) while Saimiri is a genus with paedomorphic (child like) traits. Yet, the whole clade Cebinae is characterized by a unique combination of very high pre-natal growth rates and relatively slow post-natal growth rates when compared to the rest of the NWM. Morphologically Cebinae can be considered paedomorphic in relation to the other NWM. Geometric morphometrics allows the precise separation of absolute size, shape variation associated with size (allometry), and shape variation non-associated with size. Interestingly, and despite the fact that they were extracted as independent factors (principal components), evolutionary allometry (those differences in allometric shape associated with intergeneric differences) and ontogenetic allometry (differences in allometric shape associated with ontogenetic variation within genus) are correlated within these two genera. Furthermore, morphological differences produced along these two axes are quite similar. Cebus and Saimiri are aligned along the same evolutionary allometry and have parallel ontogenetic allometry trajectories.

Conclusion

The evolution of these two Platyrrhini monkeys is basically due to a size differentiation (and consequently to shape changes associated with size). Many life-history changes are correlated or may be the causal agents in such evolution, such as delayed on-set of reproduction in Cebus and larger neonates in Saimiri.     

Observations on two types of neotropical primate intertaxa associations

During a socioecological field study of Colombian spider monkeys, data were collected on spatial associations and social and ecological interactions among free-ranging Ateles belzebuth, Alouatta seniculus, Cebus apella, and Saimiri sciureus. The most frequently observed associations occurred between groups of squirrel and capuchin monkeys. Saimiri-Cebus associations were seen at all times of day and year, but no intertaxa play, passive body contact, or grooming interactions were observed. The Saimiri-Cebus association was paralleled by one between Saimiri and the small hawk, Harpagus bidentatus, and sometimes other insectivorous birds. These associations may be based in part on a complex balance of both mutual and one-sided foraging advantages. Less frequent associations between Ateles and Alouatta were based on mutual attraction to specific fruiting trees or contacts occurring on travel routes. Unlike the more frequently observed associations between Saimiri and Cebus, those between Ateles and Alouatta included both positive and negative interactions; for example, mutual play, grooming, and olfactory investigation as well as threats, chases, and supplantations.     

Adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus)

We examined adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus), a species in which close relatedness among philopatric males and high paternity uncertainty should minimize both aggressive and affiliative behavior by males toward infants. As expected, male-infant interactions were extremely rare during this 10-month field study. None were observed in over 236 hr of observation on a cohort of six infants (0 – 13 months old). The 29 interactions observed ad lib involved 5 of the 6 infants and 9 of the 16 adult males in the group. All of the male-infant interactions were affiliative, but extremely brief. The median duration of interactions was only 0.33 min, and none lasted longer than 1.52 min. Infants always initiated, and nearly always terminated, their interactions with adult males. The indifference that appears to characterize muriqui male-infant interactions differs from the ways in which other male primates interact with infants when protection of genetic interests or investment in mating effort are involved.     

Reconciliation in the Spotted Hyena (Crocuta crocuta)

Theory predicts that it should often be in the best interests of gregarious animals to repair social bonds damaged by within-group conflict. Indeed, reconciliation in many primates takes the form of affiliative behavior occurring shortly after a conflict. Here we inquired whether reconciliation also occurs among spotted hyenas ( Crocuta crocuta ), gregarious carnivores whose social lives share much in common with those of cercopithecine primates. In a large group of free-living hyenas in Kenya, we used focal animal observations to monitor rates at which various affiliative behaviors occurred before and after dyadic aggressive interactions. An affiliative behavior was identified as having a conciliatory function only if it occurred more frequently after than before fights, and if it was also associated with reduced rates of aggression between former opponents during the post-conflict interval. Of all affiliative behaviors monitored, only two types satisfied both these criteria: greeting behavior and non-aggressive approach. Over 72% of conciliatory behaviors occurred within the first five minutes after a fight, and hyenas reconciled after 14.6% of 698 fights. Mean conciliatory tendency (CT) for individual hyenas was 11.3%. Hyenas exhibited higher CTs when they were recipients (victims) of aggression than when they were aggressors, and they showed higher CTs in interactions with non-kin than with kin. Conciliatory tendencies did not vary with age–sex classes of opponents or with rank distance between opponents . Conciliatory tendency in spotted hyenas fell at the low end of the CT range observed among primates.     

Importance of cooperation and affiliation in the evolution of primate sociality

The idea that competition and aggression are central to an understanding of the origins of group‐living and sociality among human and nonhuman primates is the dominant theory in primatology today. Using this paradigm, researchers have focused their attention on competitive and aggressive behaviors, and have tended to overlook the importance of cooperative and affiliative behaviors. However, cooperative and affiliative behaviors are considerably more common than agonistic behaviors in all primate species. The current paradigm often fails to explain the context, function, and social tactics underlying affiliative and agonistic behavior. Here, we present data on a basic question of primate sociality: how much time do diurnal, group‐living primates spend in social behavior, and how much of this time is affiliative and agonistic? These data are derived from a survey of 81 studies, including 28 genera and 60 species. We find that group‐living prosimians, New World monkeys, Old World monkeys, and apes usually devote less than 10% of their activity budget to active social interactions. Further, rates of agonistic behaviors are extremely low, normally less than 1% of the activity budget. If the cost to the actors of affiliative behavior is low even if the rewards are low or extremely variable, we should expect affiliation and cooperation to be frequent. This is especially true under conditions in which individuals benefit from the collective environment of living in stable social groups. Am J Phys Anthropol 128:84–97, 2005. © 2005 Wiley‐Liss, Inc.