Selective attention toward female secondary sexual color in male rhesus macaques

Pink-to-red anogenital and facial sexual skin occurs in females of many primate species. Since female sexual skin color varies with reproductive state, it has long been assumed that color acts to stimulate male sexual interest. Although there is supportive evidence for this as regards anogenital skin, it is unclear whether this is also the case for facial sexual skin. In this study we experimentally manipulated digital facial and hindquarter images of female rhesus macaques (Macaca mulatta) for color within the natural range of variation. The images were presented to adult male conspecifics to assess whether the males exhibited visual preferences for red vs. non-red female coloration, and whether preferences varied with anatomical region. The males displayed significantly longer gaze durations in response to reddened versions of female hindquarters, but not to reddened versions of faces. This suggests that female facial coloration may serve an alternative purpose to that of attracting males, and that the signal function of sexual skin and the intended recipients may vary across anatomical regions.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.     

Pregnancy coloration in macaques may act as a warning signal to reduce antagonism by conspecifics

Instances of bright, hormonally induced coloration among females during gestation have been reported in a few reptile and primate genera. Gravid coloration in lizards has been linked to female aggression but the influence of color changes associated with pregnancy has not yet been experimentally pursued for primates. As a first step to determine whether the crimson to magenta hues common to pregnancy coloration in rhesus macaques (Macaca mulatta) contains information, to which conspecifics of either sex attend, we evaluated whether male and female rhesus macaques discriminate between pregnant and non-pregnant female faces. To these ends, we presented 19 adult rhesus macaques with color-manipulated digital images of female faces where pregnancy coloration was present or absent, and measured visual attention and behavioral reactions. Males were significantly more attentive to female faces with pregnancy coloration over those without pregnancy coloration. Both sexes engaged in higher levels of appeasement behavior toward stimulus with pregnancy coloration, and males showing signs of anxiety did so exclusively when exposed to faces with pregnancy coloration. Our results suggest that pregnancy coloration might be an attention grabbing stimulus to males and a warning stimulus to both male and female rhesus macaques. The findings provide a comparative perspective on the use of color in intra-specific communication, and suggest similarity in female similarity in signalling properties in distantly related taxa.     

Females Pay Attention to Female Secondary Sexual Color: An Experimental Study in <Emphasis Type="Italic">Macaca mulatta</Emphasis>

Researchers have long considered the color of female sexual skin to play a role in attracting or inciting competition among males, or both; however, females may also use color in intrasexual communication. To assess this possibility, we examined whether variation in same-sex sexual skin color is salient to female rhesus macaques (Macaca mulatta). We exposed adult females to computerized images of conspecific female faces and hindquarters manipulated for color (red vs. non-red), within the natural range of color variation. Females visually attended more to both reddened faces and hindquarters over the non-red counterparts. We conclude that female color might be biologically meaningful to other females.     

Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice

Male animals of many species use conspicuous coloration to attract mates. Among mammals, primates possess the most brilliant secondary sexual coloration. However, whether colour plays a part in primate female mate choice remains unknown. Adult male rhesus macaques undergo a hormonally regulated increased reddening of facial and anogenital skin during their mating season. We experimentally investigated whether red male facial coloration is preferred by simultaneously presenting female rhesus macaques (n = 6) with computer-manipulated pale and red versions of 24 different male faces. The duration and direction of gaze were measured to discern visual preferences. Females exhibited preferences for the red versions of male faces. It is proposed that male coloration might provide a cue to male quality.     

Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques?

In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogen-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30-40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females' fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.     

Females without infants: mating strategies in two species of captive macaques

Bonnet (Macaca radiata) and rhesus (Macaca mulatta) macaque females were observed during the breeding season to evaluate differences in mating strategies between females without infants and females with dependent offspring. Rhesus nonmothers participated in consortships earlier in the breeding season and initiated and received more approaches with adult males than rhesus mothers did. Bonnet nonmothers entered estrus earlier, began copulating earlier, and approached and presented to adult males more often than bonnet mothers did. Interacting with males frequently and early in in the breeding season may improve nonmothers' chances of conceiving and bringing offspring to term, with little competition from mother peers.     

Effects of nonmaternal restraint on the vocalizations of infant rhesus monkeys (Macaca mulatta)

This study explored the effects of restraint by females other than the mother on the vocalizations of infant rhesus macaques (Macaca mulatta) in a captive social setting. In this species, females are very attracted to young infants and will frequently approach, groom, and hold the infant. Incompetent handling, abusive behavior, or extended periods away from the mother that prevent the infants from nursing represent potentially significant risks for infants. Vocal responses to such risky conditions appear to be the infants' only means to promote a return to their mothers. We examined the association between the severity of the threat posed to the infant and the nature of its vocal response to restraint, and whether the infants' calls influenced the behavior of their mothers or captors. The results suggest that situations posing greater risks for the infants, i.e., longer periods of restraint, were associated with a greater use of noisy screams. Furthermore, mothers' responding was associated with a greater use of noisy screams as well. The mothers' reactions, however, could be described as cautious, and consisted mostly of closer monitoring; such tempered response might be related to the risk of injury to the infant that could result from a more forceful and direct attempt at retrieval.     

Delayed imitation of lipsmacking gestures by infant rhesus macaques (Macaca mulatta)

Human infants are capable of accurately matching facial gestures of an experimenter within a few hours after birth, a phenomenon called neonatal imitation. Recent studies have suggested that rather than being a simple reflexive-like behavior, infants exert active control over imitative responses and 'provoke' previously imitated gestures even after a delay of up to 24 h. Delayed imitation is regarded as the hallmark of a sophisticated capacity to control and flexibly engage in affective communication and has been described as an indicator of innate protoconversational readiness. However, we are not the only primates to exhibit neonatal imitation, and delayed imitation abilities may not be uniquely human. Here we report that 1-week-old infant rhesus macaques (Macaca mulatta) who show immediate imitation of a lipsmacking gesture also show delayed imitation of lipsmacking, facilitated by a tendency to refrain from lipsmacking toward a still face during baseline measurements. Individual differences in delayed imitation suggest that differentially matured cortical mechanisms may be involved, allowing some newborns macaques to actively participate in communicative exchanges from birth. Macaque infants are endowed with basic social competencies of intersubjective communication that indicate cognitive and emotional commonality between humans and macaques, which may have evolved to nurture an affective mother-infant relationship in primates.     

Children aged 7–9 prefer cuteness in baby faces,and femininity in women's faces

Infant facial features are typically perceived as “cute,” provoking caretaking behaviours. Previous research has focused on adults' perceptions of baby cuteness, and examined how these perceptions are influenced by events of the adult reproductive lifespan, such as ovulation and menopause. However, globally, individuals of all ages, including pre-pubertal children, provide notable proportions of infant care. In this study, we recruited participants in and around northern England, and tested 330 adults and 65 children aged 7–9 using a forced-choice paradigm to assess preferences for infant facial cuteness in two stimulus sets and (as a control task) preferences for femininity in women's faces. We analysed the data with Hierarchical Bayesian Regression Models. The adults and children successfully identified infants who had been manipulated to appear cuter, although children's performance was poorer than adults' performance, and children reliably identified infant cuteness in only one of the two infant stimuli sets. Children chose the feminised over masculinised women's faces as more attractive, although again their performance was poorer than adults' performance. There was evidence for a female advantage in the tasks: girls performed better than boys when assessing the woman stimuli and one of the infant stimulus sets, and women performed better than men when assessing one of the infant stimulus sets. There was no evidence that cuteness judgements differed depending upon exposure to infants (children with siblings aged 0–2; adults with a baby caregiving role), or depending upon being just younger or older than the average age of menopause. Children and grandparents provide notable portions of infant caretaking globally, and cuteness perceptions could direct appropriate caregiving behaviour in these age groups, as well as in adults of reproductive age.     

Testicular function and Scrotal coloration in patas monkeys

Patas monkeys ( Erythrocebus patas ) have aquamarine-coloured scrota, but data are unavailable regarding the potential connection between changes in scrotal coloration and testicular function. In the rhesus monkey ( Macaca mulatta ), seasonality of mating is accompanied by an intensification of red colour of the scrotum and a doubling of testicle size. A one-year study of male patas monkeys was undertaken in order to examine potential seasonal correlates of testicular function and scrotal colour. Increases in testosterone concentrations and testicular volume occurred during the mating season in adult males, but scrotal colour was fairly uniform throughout the year. Neither age, body weight, nor health influenced scrotal colour. These findings contradict the suggestion that the sex skin of seasonally breeding primates will become more intense during the mating season as a result of elevations in steroid hormone levels. Evidence from field studies in Africa suggest that the colour is part of a constellation of traits involved in male competition for mates.     

Social behavior in aged rhesus macaques

This study investigated the relationship between chronological age and social behavior in 42 adult male and female rhesus macaques (Macaca mulatta) in three specific areas: social interactions, social roles, and social networks. While both old males and old females share behavioral differences associated with senescence, this study reports that old females and old males are distinct in their social behaviors, both from each other and from other adults. Many of these differences appear progressive across age classes, e.g., declining across age classes in females and increasing across age classes in males. Old females are less social and have smaller social networks than other females, while the opposite was found to be true of old males. An explanation for the sex-based differences in aged social behavior and social networks reported in this study may originate in rhesus matrifocal social structure.     

Baby Schema in Infant Faces Induces Cuteness Perception and Motivation for Caretaking in Adults

Ethologist Konrad Lorenz proposed that baby schema ('Kindchenschema') is a set of infantile physical features such as the large head, round face and big eyes that is perceived as cute and motivates caretaking behavior in other individuals, with the evolutionary function of enhancing offspring survival. Previous work on this fundamental concept was restricted to schematic baby representations or correlative approaches. Here, we experimentally tested the effects of baby schema on the perception of cuteness and the motivation for caretaking using photographs of infant faces. Employing quantitative techniques, we parametrically manipulated the baby schema content to produce infant faces with high (e.g. round face and high forehead), and low (e. g. narrow face and low forehead) baby schema features that retained all the characteristics of a photographic portrait. Undergraduate students (n = 122) rated these infants' cuteness and their motivation to take care of them. The high baby schema infants were rated as more cute and elicited stronger motivation for caretaking than the unmanipulated and the low baby schema infants. This is the first experimental proof of the baby schema effects in actual infant faces. Our findings indicate that the baby schema response is a critical function of human social cognition that may be the basis of caregiving and have implications for infant–caretaker interactions.     

Surgical correction of genital prolapse in three rhesus monkeys

Three adult female rhesus monkeys (Macaca mulatta) in a breeding colony of approximately 75 adult females developed a clinical condition characterized by protrusion of the cervix through the vulva during pregnancy and/or following parturition. The Gilliam round-ligament uterine ventro-suspension procedure (hereafter called the Gilliam uterine suspension or uterine suspension procedure) was used to return the cervix to a normal anatomical position. Following the procedure, one female delivered a normal live infant, but reprolapsed. After a second suspension procedure, she again became pregnant and delivered a normal live infant without a reoccurrence of the prolapse. A second animal never became pregnant despite repeated breedings to different males for two years. The third animal became pregnant twice following the procedure. The first pregnancy terminated in abortion at two months of gestation, while the second pregnancy ended in an apparent dystocia, necessitating a cesarean section and delivery of a dead fetus. The animal died post-operatively. This surgical procedure successfully salvaged one of these animals which otherwise had no reproductive future.     

Corneal biometrics of the rhesus monkey (Macaca mulatta)

Keratometry, retinoscopy, horizontal diameter, and pachymetry were measured in adult and infant rhesus monkeys (Macaca mulatta). The adult monkeys had a mean corneal thickness of 0.47 +/- 0.03 mm (+/- standard deviation), corneal diameters of 10.6 +/- 0.5 mm, keratometry values of 51.90 +/- 1.61 diopters, and subjective refractions of 0.48 +/- 2.36 diopters. Female adult monkeys had smaller corneal diameters by 0.06 mm (P = .02) and steeper corneas by 0.77 diopters (P = .04). Infant female monkeys also had steeper corneas by 2.37 diopters (P = .05). No significant differences were found between right and left eyes in either adult or infant monkeys.     

Successful behavioral strategy to unite mother and infant rhesus monkeys (Macaca mulatta) after cesarean delivery

Developmental studies of pre‐ to postnatal continuities in rhesus monkeys sometimes require infants be reared with their mothers. However, complications during pregnancy or experimental designs may require cesarean delivery. Owing to lack of published information on this subject, strategies are needed to introduce mothers to their infants following cesarean delivery. Using positive and negative reinforcement techniques we attempted to unite six infant rhesus macaques, Macaca mulatta, to their mothers following c‐sections. For our seventh subject, we attempted to cross‐foster an infant onto an unrelated female after she had undergone a cesarean surgery for a late‐term spontaneous abortion. The mothers varied in age, parity, previous postnatal mothering experience with infants, housing earlier to delivery, and housing subsequent to introduction. Although there were large individual differences among the mother–infant pairs, all seven introductions were successful. The mothers learned to accept and care for their infants from the continuous application of operant conditioning techniques. These data suggest that mother‐rearing following cesarean section is a realistic possibility whether required for clinical reasons or for proper experimental control. Furthermore, the ability to successfully mother‐rear infants produced from cesarean delivery lessens the impact this potential confound of not being reared by their mothers exerts on many types of developmental studies. Am. J. Primatol. 71:510–522, 2009. © 2009 Wiley‐Liss, Inc.     

Pheromonal Recognition of Females Takes Precedence over the Chromatic Cue in Male Iberian Wall Lizards Podarcis hispanica

Sex recognition is based on colour signals in many species of lizards. However, olfactory stimuli are also clearly involved, and many species might rely more on chemoreception. We aimed to examine whether colour pattern or odours, or both, are used in sex recognition and which cues elicit courtship of females by males of the lizard Podarcis hispanica . We experimentally manipulated the coloration and odour of female P. hispanica , thereby creating groups with all combinations between coloration and odour of males and females. Using data from staged encounters, we compared the responses of resident males to manipulated and unmanipulated individuals (males and females). Responding males reacted significantly more aggressively to female intruders with male odours, independently of their coloration. Nevertheless, coloration seemed to be important in long-distance sex recognition since, in the first minutes, females painted as females received a lower number of aggressive responses. Both colour and odour were important in eliciting male courtship. However, females painted as females and with female odours were preferentially courted. Comparisons with unmanipulated male and female intruders agreed with these expectations. Therefore, at close range, odoriferous cues seem to be more important than colour patterns in sex recognition, but female coloration is also useful at long range to deter the aggressive response of males and to elicit courtship in conjunction with odours.     

Carbon monoxide excretion as an index of bilirubin production in rhesus monkeys

The role of increased heme catabolism in neonatal hyperbilirubinemia was investigated in rhesus (Macaca mulatta) neonates through the measurement of carbon monoxide excretion rates (VECO), blood carboxyhemoglobin content (HbCO), and plasma bilirubin concentrations. Neonatal values were compared to those of adult rhesus monkeys. These indices of bilirubin production responded appropriately to administration of NEM-damaged erythrocytes and tin protoporphyrin. Our results indicate that VECO measurements are a valid index of changes in bilirubin production in the newborn rhesus monkey.     

Measuring temperament in rhesus macaques: consistency and change in emotionality over time

This study of rhesus macaques (Macaca mulatta) investigated whether individual differences in emotionality, as measured by scratching frequencies, are stable over time and across seasons. Five adult females living in captive social groups were observed during two consecutive birth seasons and five females during the birth and the mating season. Scratching frequencies were higher during the birth than during the mating season, suggesting that the presence of infants was associated with elevated emotionality. Individual differences in scratching frequencies remained stable across two consecutive birth seasons, but there was no significant correlation between scratching frequencies in the birth and in the mating season. These findings suggest that, under certain circumstances, individual differences in emotionality are consistent over time and that scratching may be used as a non-invasive indicator of temperament.