Infants as a commodity in a baboon market

We used data from adult female chacma baboons, Papio cynocephalus ursinus, to provide the first test of hypotheses on interchange trading and the structure of a biological market (Noë & Hammerstein 1994, Behavioral Ecology and Sociobiology,35, 1-11) within a primate group. The interchange commodities selected were grooming and handling of infants less than 3 months of age. Patterns of grooming in relation to infant handling showed strong evidence for interchange. Grooming for infant access was initiated by potential handlers and was significantly likely to be nonreciprocated. More critically, the data show that infant ‘supply’ created a market effect: grooming bout duration (the price ‘paid’ for handling) was inversely related to the number of infants present in the group. In addition, there was an inverse relationship between grooming bout duration and the rank distance between mothers and handlers, suggesting that higher-ranking mothers could demand a higher price for infant handling. Where rank distance was high, females were able to handle infants without grooming. Dominance could thus be used to disrupt the infant market effect. If biological markets models are to be fully applicable to primate groups (and those of other social mammals) then the potentially distorting effect of dominance needs to be incorporated into the framework. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Grooming and Infant Handling Interchange in <Emphasis Type="Italic">Macaca fascicularis</Emphasis>: The Relationship Between Infant Supply and Grooming Payment

Female long-tailed macaques are attracted to infants and frequently groom mothers bearing them. Such grooming often involves the groomer contacting the infant and may be a trade of grooming for infant handling. To identify if grooming and infant handling are directly traded, I collected samples on times after female-to-mother grooming and on interactions in which a female groomed a mother and contacted her infant. I determined that grooming tended to promote an exchange with infant handling and that the supply of available infants was related to how long a female groomed a mother. Grooming interactions were longer when infants were scarce in the surrounding social environment than when they were abundant, indicating a possible supply-and-demand effect. This supports that grooming may be payment for infant handling. Grooming-infant handling interchanges tended to be unidirectional as mothers usually did not reciprocate grooming. Instead, infant contact occurred. A larger proportion of grooming-infant handling interchanges involved younger infants, but infant age did not seem to influence grooming durations. The length of female-to-mother grooming had no observable effect on handling time. Lower-ranked females groomed higher-ranked mothers and their infants longer than vice versa. Moreover, it was possible to predict up-rank grooming via supply and demand better than down-rank grooming. There was no observable influence of kinship on grooming-infant handling interchange. These results support the conclusion that grooming and infant handling may be traded. Grooming promoted infant handling, while supply and rank predicted the grooming payment a female would offer to access an infant.     

Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana)

Social grooming is a common form of affiliative behavior in primates. Biological market theory suggests that grooming can be traded either for grooming or other social commodities and services. When no other services are exchanged, grooming is predicted to be approximately reciprocated within a dyad. In contrast, the amount of reciprocal grooming should decrease as other offered services increase. We studied grooming patterns between polygamous male and female in golden snub-nosed monkeys (Rhinopithecus roxellana) from the Qinling Mountains of central China and found that about 29.7% of grooming bouts were reciprocated. However, the durations of grooming bouts offered and returned was asymmetrical within dyads. In bisexual dyads, more grooming was initiated by females than males, which became more pronounced as the number of females per one-male unit increased. The rate of copulation per day for each female was positively correlated with the total duration of grooming time females invested in males.. Females without an infant (non-mothers) directed more grooming towards females with an infant (mothers) and were significantly more likely to be non-reciprocated. There was a significant negative relationship between non-mother and mother grooming duration and the rate of infants per female in each one-male unit. High-ranking females also received more grooming from low-ranking females than vice versa. The rate of food-related aggressive interactions was per day for low-ranking females was negatively correlated with the duration of grooming that low-ranking females gave to high-ranking females. Our results showed that grooming reciprocation in R. roxellana was discrepancy. This investment-reciprocity rate could be explained by the exchange of other social services in lieu of grooming.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Intra-troop affiliative relationships of females with newborn infants in wild ring-tailed lemurs (Lemur catta)

To determine how the birth and development of infants influence their mothers' social relationships with other adult troop members, we observed two free-ranging troops of ring-tailed lemurs (Lemur catta) at the Berenty Reserve, Madagascar. The number of acts of affiliative contact that the mothers received from other adult troop members during the first and second months of infant life were significantly higher than those before they gave birth, and the values during the third month were as low as that before giving birth. Two mothers received acts of affiliative contact less frequently after their infants died, compared with the values while the infants were alive. On the other hand, more than 95% of all acts of licking of infants by adult troop members other than their mothers occurred when the infants were in contact with their mothers. These findings suggest that infants per se and mothers per se were not attractive, but rather the mother-infant pair was attractive to other troop members. Acts of infant-licking were observed in almost all mother-mother pairs and mother-non-mother adult female pairs, and in two thirds of mother-adult male pairs. Moreover, the frequency of infant-licking was not affected by female parity, female and male dominance rank, or infant sex. Therefore, acts of infant-licking, which are widespread among troop members, may function to make or maintain stable social relationships.     

Weaving a tight social net: Allogrooming in free-ranging female langurs (Presbytis entellus)

We studied grooming among adults of a one-male multifemale troop of free-ranging Hanuman langurs (Presbytis entellus)living near Jodhpur, India, for 9 years. The 11–13 females devoted about 6% of their day to allogrooming. Adult males, whose tenures averaged 2.2 years, were transient figures in the troop's history, as reflected by their rather peripheral role in the grooming network. Females groomed males 4–40 times more frequently (1006 episodes) than vice versa- (176 episodes). Adult females received 97% of all grooming from other adult females (6655 episodes). Although females exhibited an age- inversed dominance hierarchy, they did not compete for grooming access to particular troop mates. Dyads of all possible rank differences occurred as frequently as expected: 51% of grooming was directed up the hierarchy and 49% down it. Young, high- ranking individuals gave and received significantly more grooming than the oldest, low- ranking females did. The pattern seemed to be influenced by kin selection because of the presumably high degree of female relatedness. They invested most in troopmates with the highest reproductive value, i.e., the youngest individuals. This trend was coupled with a preference of closest kin (mothers and daughters). Reciprocity was the outstanding feature since all adult females groomed and were groomed by all others. Such a tight social net might establish the necessary cohesion during frequent territorial disputes with neighboring troops.     

Benefits to Female Helpers in Wild Rhinopithecus roxellana

To assess what female Sichuan snub-nosed monkeys (Rhinopithecus roxellana) gain from allowing others to care for their infants, we collected behavioral data on 12 mother-infant dyads at Zhouzhi National Nature Reserve in the Qinling Mountains, China. Mothers’ feeding time significantly increased when infants were cared for by other group members versus when they were cared for by the mothers themselves. The time mothers spent autogrooming and receiving grooming also increased when they were temporarily relieved of maternal duties; however, mothers did not groom other individuals more when they were not encumbered by infants. There are several benefits that mothers gain from having helpers care for their infants: They gain more time to feed and thus increase their feeding efficiency. Mothers have more time to engage in hygienic and maintenance activities because they autogroom and receive allogrooming more. Lastly, mothers save energy when their infants are with helpers. Wild Sichuan snub-nosed monkey mothers meet their basic survival and maintenance needs because of helping behavior.     

The ontogeny of social relationships with group companions among free-ranging infant rhesus monkeys II. Differentiation and attractiveness

Infants are frequently with their mothers when troop members initiate interaction with them. To what extent are the infants' companions attracted specifically to them rather than to the mother? A simple method is presented for approaching this question and for assessing the extent to which the relationships of 11 free-ranging rhesus (Macaca mulatta) infants on Cayo Santiago have acquired qualities independent of (differentiated from) those of the mother. Companions of all ages tend to be attracted specifically to infants between 1 and 14 weeks of age and not simply to their mothers. However, this tendency is less marked for sibling companions than for more distantly related companions. No differences are found between infants of high- and low-ranking mothers. Infantile attractiveness is not necessarily sustained when infants are 17 to 30 weeks of age. The degree to which relationships with infant companions and with older female companions have, differentiated by 17 to 30 weeks is negatively related to the companion's age. Infants show early and increasingly marked tendencies to develop differentiated relationships with one another; however, they show no signs of doing so with adult female companions by 30 weeks of age.     

Socio-maternal behaviors in response to an infant birth inColobus guereza

A number of social behaviors were observed in a captive troop ofColobus guereza on a regular basis for eight months. These included clasping and related behaviors, forward mounts, rear mounts, presents, troop positions during rest periods, infant transfers and attempted transfers, play, and grooming. During the observation period two significant events occurred: a re-introduction of a mother and her juvenile female, and the birth of an infant to a resident female. These events caused an increase in certain adult behaviors indicating a relationship of them with similar behaviors done between mothers and infants. This similarity seemed to indicate the co-evolution of “maternal” behaviors for use in adult social interactions and the phenomenon of infant transfer or sharing. The maternal and socio-maternal behaviors and their infantile precursors are then discussed in relation to the ontogeny of behavioral forms, the ontogeny of motivation in such behaviors, and the idea of infantile regression during development and in adult life.     

Take-over and infanticide in South Indian Hanuman langurs (Presbytis entellus)

A take-over and infanticide were observed in a South Indian population of Hanuman langurs (Presbytis entellus). A one-male, bisexual troop of langurs (Troop B1) was attacked by a band of two adult males and one subadult male. During the take-over, the resident male and one elderly female were driven from the troop. The youngest infant, about two months old, was fatally wounded by an attack from the dominant incoming male (S1). However, other young infants in Troop B1 were left unharmed. All three incoming males remained in Troop B1 but the troop appeared to remain functionally one-male, as S1 did not allow the other adult male to copulate. There was no sign that S1 attempted to eject the other two males from troop B1. © 1993 Wiley-Liss, Inc.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Maternal responses to dead and dying infants in wild troops of ring-tailed lemurs at the Berenty Reserve,Madagascar

We describe responses of seven mothers and other troop members to dead and dying infants in several troops of ring-tailed lemurs(Lemur catta) at the Berenty Reserve, Madagascar. In contrast to mothers in simian species, ring-tailed lemur mothers rarely carried their dying, immobile or dead infants. However, they sniffed, licked, and touched them even after they had died. While the dying infants were still peeping, their mothers remained near them, and 15 to 76 min after the infants ceased to peep, they were left by their mothers. Six of the seven mothers returned to their dead infants several times within the first few hours after they had left them. All seven mothers gave repeated calls, such as “mew” and “pyaa,” when they were separated from either their dead infants or other troop members or both. Thus, each mother exhibited some form of maternal behavior toward her dead infant for hours after its death. These results indicate that there may not be a great gap in terms of maternal affection between simian and prosimian mothers. We also discuss visuospatial memory ability in ring-tailed lemurs and the causes of the infants’ deaths.     

The play partners of immature baboons

In a troop of free-ranging baboons, infants played predominantly with each other, and played most with the infant of the highest-ranking female in their mothers' subgroup. The frequency of infant play appeared to be affected both by age and by the number and ages of other infants in the troop. Juveniles and subadults played more with their siblings than with other animals of their siblings' age. Juvenile and subadult females played primarily with infants, and played most with infants whose mothers ranked higher than their own. Juvenile and subadult males played most with like-sexed peers. The distribution of play partners among immatures illustrates how demographic and maturational factors, as well as those related to kinship, may reinforce or counteract one another during development.     

The variable social organization of hanuman langurs(Presbytis entellus), infanticide,and the monopolization of females

Data from 24 wild populations of hanuman langurs (Presbytis entellus)in south Asia are used to test hypotheses seeking to explain variation in troop structure and the incidence of infanticide. The occurrence of infanticide is associated with a one-male troop structure and not with a high density. The density, predation, and economic-advantage hypotheses, as explanations for the occurrence of one-male and multimale troops, are not supported by the review. However, the monopolization hypothesis is not contradicted; the number of adult males per troop is significantly correlated with troop size and with the number of adult females per troop. Therefore it is suggested that a one-male troop structure will arise if a male is able to monopolize a group of females, a multimale troop if he cannot. One-male troops may predispose to infanticide because of high variance in male mating success and high intermale competition between groups rather than within troops. If female dispersion determines troop structure, it is speculated that females could manipulate males to form a multimale society if the advantages in terms of infant survival and intertroop conflict exceeded the costs in terms of not producing infanticidal “sexy sons.”     

Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei)

Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multi-male groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females’ social partner choice than paternity. Older infants (2–3 years) in multi-male groups mirrored their mothers’ preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle.     

Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus Bieti)

Background

Allomaternal nursing, common in several species of social mammals, also has been reported in nonhuman primates. However, the function of this behavior in enhancing infant survivorship remains poorly understood.

Methodology and Principal Findings

The study was conducted on a free-ranging group of the Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Natural Reserve. Direct observation and ad libitum sampling were used to record allocare behavior during a 20 month field study. R. bieti exhibits a multilevel social organization in which a large single troop, consisting of over 100 individuals, is divided into many one-male units (OMUs: 6∼41). These OMUs coordinate their daily activities, and feed, forage, travel, and rest together. Here we report on one case of infant temporary adoption in which an adult female from one OMU engaged in allomaternal nursing and cared for an infant from a different OMU of the same troop. This event began when the mother and her five-month-old infant were found to became separated accidentally. The victim infant was observed staying in another OMU. Over the next several days we observed a lactating female in the new OMU to care for and nurse both her infant and the immigrant infant, who also was tolerated by and cared for by the harem male.

Conclusions and Significance

Our findings suggest that lactating primate females are primed to care for young infants and, that the misdirected parental care hypothesis may offer the strongest explanation for allomaternal nursing in R. bieti.     

Female dominance and female social relationships among yellow baboons (Papio hamadryas cynocephalus)

Adult females in a female-bonded, cercopithecine species such as baboons are characterized by hierarchically ranked matrilines, i.e., female offspring assume rankings just beneath those of their mothers. In this system of closely ranked matrilines, a female should engage in significantly more affiliative interactions with those individuals who are closely ranked to herself than with those individuals who are more distantly ranked. We examine the hypothesis that females in this troop of feral yellow baboons (Papio hamadryas cynocephalus) who are closely ranked will also show close social affiliation. We collected focal data on 23 feral, adult female subjects (253 possible dyads) over approximately 1 year at the Tana River National Primate Reserve, Kenya. Following Bramblett's [Behav Brain Sci 4: 435, 1981] method of dominance tabulation and utilizing a modified version of Smuts' [Sex and friendship in baboons, Hawthorne: Aldine Publishing Co., 1985] preferred partner index, we describe and compare the dominance matrix and hierarchy, preferred proximity partner and grooming partner sociograms, and the social networks of these 23 focal females. Over 1,400 interactions were utilized in the dominance tabulations, 41 statistically significant proximity partner preferences were documented, and 100 grooming dyads were recorded. We examine both partners' ranks and the presence of an infant as possible factors influencing proximity and grooming partner preferences. We find that in this population there is no direct correspondence between females' ranks and their affiliation partners. Neither proximity nor grooming preferences are consistently predictable from partners' ranks. While proximity preferences were not significantly influenced by the presence of an infant, grooming partner preferences were. Females with infants had more grooming partners and were more often involved in unidirectional grooming relationships as the recipients than were females without infants. We conclude that females' dominance rankings are not good predictors of either proximity partner or grooming partner preferences and that the presence of an infant does have a significant impact on grooming partner preferences in this population.     

Social relationships of nulliparous young adult females beyond the ordinary age of the first birth in a free-ranging troop of Japanese macaques (Macaca fuscata)

We describe the social relationships of young adult female Japanese macaques (Macaca fuscata) in a free-ranging troop in Arashiyama, Kyoto, Japan, who remained nulliparous beyond the ordinary age of first birth because of contraceptive administration. We observed 12 young nulliparous adult females (6–9 years old) for 270 h and 10 min from 2 February to 5 October 2010. The majority maintained close relationships with their mothers through proximity and grooming, whereas a few had very infrequent social interactions with their mothers. Most had asymmetrical grooming relationships; the grooming they received from unrelated adult females was less than the grooming they gave. Young adult females who had less frequent interactions with their mothers by either proximity or grooming received more grooming from a larger number of unrelated adult females than did those who had more frequent social interactions with their mothers. These results indicate that most young adult females who remained nulliparous beyond the ordinary age of first birth tended to maintain close relationships with their mothers, and their grooming relationships with unrelated adult females were inversely related to the degree of closeness with their mothers.     

Changes in Variable Number of Tandem Repeats in ‘Candidatus Liberibacter asiaticus’ through Insect Transmission

Citrus greening (huanglongbing) is the most destructive citrus disease worldwide. The disease is associated with three species of ‘Candidatus Liberibacter’ among which ‘Ca. Liberibacter asiaticus’ has the widest distribution. ‘Ca. L. asiaticus’ is commonly transmitted by a phloem-feeding insect vector, the Asian citrus psyllid Diaphorina citri. A previous study showed that isolates of ‘Ca. L. asiaticus’ were clearly differentiated by variable number of tandem repeat (VNTR) profiles at four loci in the genome. In this study, the VNTR analysis was further validated by assessing the stability of these repeats after multiplication of the pathogen upon host-to-host transmission using a ‘Ca. L. asiaticus’ strain from Japan. The results showed that some tandem repeats showed detectable changes after insect transmission. To our knowledge, this is the first report to demonstrate that the repeat numbers VNTR 002 and 077 of ‘Ca. L. asiaticus’ change through psyllid transmission. VNTRs in the recipient plant were apparently unrelated to the growing phase of the vector. In contrast, changes in the number of tandem repeats increased with longer acquisition and inoculation access periods, whereas changes were not observed through psyllid transmission after relatively short acquisition and inoculation access periods, up to 20 and 19 days, respectively.     

The Genome Sequence of ‘Mycobacterium massiliense’ Strain CIP 108297 Suggests the Independent Taxonomic Status of the Mycobacterium abscessus Complex at the Subspecies Level

Members of the Mycobacterium abscessus complex are rapidly growing mycobacteria that are emerging as human pathogens. The M. abscessus complex was previously composed of three species, namely M. abscessus sensu stricto, ‘M. massiliense’, and ‘M. bolletii’. In 2011, ‘M. massiliense’ and ‘M. bolletii’ were united and reclassified as a single subspecies within M. abscessus: M. abscessus subsp. bolletii. However, the placement of ‘M. massiliense’ within the boundary of M. abscessus subsp. bolletii remains highly controversial with regard to clinical aspects. In this study, we revisited the taxonomic status of members of the M. abscessus complex based on comparative analysis of the whole-genome sequences of 53 strains. The genome sequence of the previous type strain of ‘Mycobacterium massiliense’ (CIP 108297) was determined using next-generation sequencing. The genome tree based on average nucleotide identity (ANI) values supported the differentiation of ‘M. bolletii’ and ‘M. massiliense’ at the subspecies level. The genome tree also clearly illustrated that ‘M. bolletii’ and ‘M. massiliense’ form a distinct phylogenetic clade within the radiation of the M. abscessus complex. The genomic distances observed in this study suggest that the current M. abscessus subsp. bolletii taxon should be divided into two subspecies, M. abscessus subsp. massiliense subsp. nov. and M. abscessus subsp. bolletii, to correspondingly accommodate the previously known ‘M. massiliense’ and ‘M. bolletii’ strains.