Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier?

Allonursing, the behaviour of females nursing offspring that are not their own, is relatively frequent in capuchin monkeys. Using focal-animal sampling and ad libitum observations we describe the pattern of allonursing in a wild group of tufted capuchins, Cebus nigritus (4 cohorts, 22 infants), at Iguazú National Park, north-eastern Argentina, and test several hypotheses on the adaptive value of allonursing. During 2,351 contact hours with the group (including 4,207 focal-animal samples totalizing 329 h focused on infants) we observed 39 allonursing bouts. Infants were not allonursed more frequently by close kin than by more distant allomothers. Offspring of dominant females were allonursed more frequently than those of low-ranking females. Nursing bouts were longer than allonursing bouts. Our results suggest that allonursing in tufted capuchins has a social function and is not mainly aimed at providing milk to infants.     

Reciprocity in play,grooming, and proximity in sibling and nonsibling young rhesus monkeys

Play, grooming, and proximity, and the degree to which these were reciprocated between pairs, were studied in immature sibling and nonsibling rhesus monkeys (Macaca mulatta)in four established captive groups over two seasons. “Interaction reciprocity” and “partner reciprocity” were assessed for each dyad for each of the three behaviors. In play, interaction reciprocity was based on the ratio between the play initiations by each dyad member,in grooming on the ratio between the grooming durations by each dyad member, and in proximity on the relative responsibility for proximity maintenance. Two or three most frequent (top) partners for each behavior were found for each individual. If two monkeys were among each other’s top partners, they were said to be reciprocal partners. Monkeys played with nonsiblings as much as with siblings but spent more time grooming and in proximity with siblings than with nonsiblings. Same-age nonsiblings (peers) were more frequent partners than other nonsiblings for each behavior. Siblings’ grooming interactions were more reciprocal than those of nonsiblings. There was no such effect for play and proximity. All-male dyads tended to be more reciprocal in play interactions, and all-female dyads tended to be more reciprocal in grooming interactions. In play, but not in grooming or proximity, the interaction reciprocity of reciprocal partners was higher than that of nonreciprocal dyads. It is argued that the three behaviors have similar roles in infant’s social development but they differ in the expression of this role. Hence the reciprocity patterns vary with the behavior.     

Calculated reciprocity? A comparative test with six primate species

Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject’s tendency to provide food to a partner was directly affected by the partner’s previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects’ probability to pull was not affected by the previous number of the partner’s pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.     

Effects of Relatedness,Dominance, Age,and Association on Reciprocal Allogrooming by Captive Impala

Wild impala display a highly reciprocal allogrooming system that, by virtue of its frequency and high degree of reciprocity, is unique among ungulates. A herd of 35 free-ranging captive impala provided opportunity to examine the degree of reciprocity of allogrooming exchanges and the influence of relatedness, dominance, age and association on partner preferences and distribution of grooming between allogrooming partners. As in wild impala, the exchange of allogrooming bouts in the captive impala was highly reciprocal regardless of partners. Kinship and dominance had no influence on partner preference or distribution of grooming between partners. Although mothers showed a significant preference to allogroom with their unweaned offspring, this preference practically disappeared with older offspring. Age-mates (no greater than 6 mo apart) tended to associate with one another and spatial proximity was positively correlated with grooming partner preference. It was not clear whether impala actively sought out age-mates for grooming, or randomly chose grooming partners from nearby age-mates. The failure to find a role for kinship and dominance is counter to what has generally been found in most Old World terrestrial primate studies. The absence of pronounced social influences, coupled with the known effectiveness of grooming in removing ectoparasites, suggest that a utilitarian role, especially removal of ticks, is an important function of the impala reciprocal allogrooming system.     

Time-matched grooming in female primates? New analyses from two species

The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout (‘time matching’). Models of allogrooming based on biological markets theory predict that individuals of lower dominance rank will exchange grooming for tolerance from high-rankers, and therefore an inverse relation will be found between grooming partners' dominance rank distance and how closely they match each other's grooming contributions within each bout. We used weighted logistic regression and weighted least-squares regression to test these predictions using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Only 5-7% of macaque grooming bouts, and 12-27% of capuchin grooming bouts, were reciprocated. However, (1) the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and (2) when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, although significant. These results indicate that although some form of time matching may be a general characteristic of grooming in female-bonded primate species, time matching accounts for relatively little of the variation in the distribution of grooming within bouts. We also draw attention to weighted regression as a technique that avoids pseudoreplication while using all available data.     

Sucking and allosucking duration in farmed red deer (Cervus elaphus)

Sucking duration in ungulates does not only mean milk transfer, but is also associated with maternal care in general. It seems to be a reflection of offspring demand rather than solely milk transfer rate. Thus, the objective of this study was to discriminate between sucking and allosucking (i.e. sucking non-maternal hind) behaviour in red deer according to the sucking duration.We hypothesized that: (1) calves should suck longer from their mothers than allosuck from non-maternal hinds; (2) sucking duration of calves frequently nursed by a particular non-maternal hind should be longer than that of calves occasionally allonursed; (3) sucking duration should be longer for bouts including one calf than two or more calves sucking simultaneously; (4) male calves should suck and allosuck longer than female calves; and (5) primiparous hinds should nurse and allonurse longer than multiparous hinds. We observed sucking behaviour of 25 hinds and their 38 calves (from birth until the youngest calf reached one month of age) in two seasons. We recorded 1730 sucking bouts, of which 11.62% in the first season and 4.37% in the second season were non-filial. The duration of filial sucking was significantly longer than non-filial sucking. A large individual variance in the incidence of non-filial sucking in both the calves and hinds was found. Therefore, the non-filial hind–calf pairs were categorized in two clusters according to the frequency of nursing non-filial calves for one hind in relationship to all nursing events for this hind by a cluster analysis (PROC CLUSTER, SAS). We used a general linear mixed model, GLMM (PROC MIXED, SAS) to test the influence of hind relationship to the nursed calf (filial, frequently allosucking non-filial, or occasionally allosucking non-filial pair). Sucking duration of occasionally allosucking non-filial calves was only marginally different from that of filial calves. There was no difference between the two groups of non-filial calves. Multiple sucking bouts were shorter than those with one calf. Male calves sucked longer than female calves; however, the greatest difference was recorded between frequently allosucking non-filial pairs of both sexes. Frequently allosucking non-filial males sucked the longest and differently from occasionally allosucking non-filial males. Frequently allosucking non-filial females sucked the shortest and differently from filial calves of both sexes. It is more likely that allosucking seems to be more important for male rather than female calves.Therefore, it is concluded that allosucking calves differ in their sucking behaviour and two types of allosuckers (frequent and occasional) should be taken into account when analyzing allosuckling behaviour.     

Revisiting non-offspring nursing: allonursing evolves when the costs are low

Allonursing, the nursing of another female''s offspring, is commonly assumed to have evolved through the benefits of kin selection or reciprocity. The evolution of allonursing may also be influenced by variation in the possible costs to allonurses. The relative influence of costs and benefits on the incidence of allonursing in mammals remains unexplored. We show, using comparative analyses, that where females group with kin, the presence or the absence of allonursing is not associated with further variation in relatedness. Allonursing is most common where females produce litters; here the relative investment per offspring is low, and the costs of nursing additional young are likely to be reduced. Our results suggest that variation in the potential benefits is not associated with the distribution of allonursing, but that allonursing can quickly evolve when the costs to allonurses of nursing additional offspring are low.     

Grooming, social bonding, and agonistic aiding in rhesus monkeys

An analysis of simultaneous grooming bouts in a captive group of rhesus monkeys (Macaca mulatta) failed to provide evidence of competition to groom high ranking partners. Not only were grooming supplantations rare, but the highest ranking individuals performing grooming did not groom the highest ranking animals receiving grooming. Lower ranking partners, however, did more grooming in nonkin dyads. Grooming partners aided one another in agonistic episodes, but the individual receiving the aid did not groom the individual providing the aid more than vice versa. Kin dyads did aid and groom one another at greater than expected rates, but the aider did not receive the greater proportion of grooming in the dyad. Males participated in more grooming than expected, but their grooming was not related to aiding either with regard to one another or female partners. Animals that were targeted in joint aggression, or aided against, received significantly less grooming from their opponents. A general social relationship expressed in partner preferences, social grooming, and agonistic aiding better explained the observed pattern than any model based on the exchange of services for favors in different currencies.     

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.     

Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India

In captivity, male bonnet macaques (Macaca radiata) frequently express "friendship" toward one another, including affiliative behavior such as huddling, grooming, coalitionary support, and sitting in close proximity. The purpose of this study was to determine whether wild adult male bonnet macaques also express "friendship" by investigating whether or not (1) adult male bonnet macaques have affiliative social relationships with other males, (2) the strength of social relationships varies among dyads, (3) there is time-matched reciprocity in allogrooming among dyads, and if so, whether the level of reciprocity occurs within a bout of grooming, a day, or over 2 months (the limit of this study), and (4) a correlation exists between the strength of social relationships and dominance ranks among adult males. Focal samples totaling 150 hr on all seven adult males in one study group were conducted to record both agonistic and affiliative interactions. Agonistic interactions were used to construct a dominance hierarchy, whereas affiliative interactions (sitting in proximity to within 1 m with and without grooming) were used to quantify the existence and strength of social bonds within dyads. Results show that adult male bonnet macaques had differentiated affiliative relationships with other males in their group. There was little reciprocity of grooming within a bout of grooming or within a day, but greater reciprocity over the study period of 2 months. There was no correlation between dominance ranking distance and the strength of affiliative relationship within dyads; however, within dyads lower-ranking males groomed higher-ranking males more than vice versa. This study suggests that friendships in male bonnet macaques are characterized not by immediate tit-for-tat reciprocal altruism, but by reciprocity over a longer time span, and that affiliative social relationships may be less constrained by agonistic relationships than is the case in more despotic species of macaques.     

Infant handling in wild Cebus capucinus: testing bonds between females?

The evolved functions, if any, of infant handling (IH) by female primates remain unclear for many species. I tested a new hypothesis, that IH tests social bonds between adult females, using data on a group of wild white-faced capuchins. I also tested the nonadaptive, learning-to-mother, reciprocity, harassment and alliance-formation hypotheses. Focal subjects were the mothers of 10 infants that ranged in age from 0 to 90 days. The behaviours comprising IH (inspecting, nuzzling, sniffing, and a distinctive vocalization) differed from typical maternal behaviour. Nulliparous females engaged in no more IH than did parous females. The median frequency of rough handling was zero, kidnapping was not observed, and maternal restraint of infants was extremely rare. Infant handling rate was unrelated to the relative dominance ranks of the mother and the handler. Females tended to handle the infants of females with which they groomed and formed aggressive coalitions more frequently. Dyadic IH rates were not correlated with rates of allonursing when the infants were older than 90 days of age. There was no evidence for reciprocal exchanges of IH between females. Mother-terminated IH bouts were longer when the mother had groomed the handler more frequently before the infant's birth. Based on these findings, the learning-to-mother, reciprocity and harassment hypotheses are unsupported for this species. Some support exists for the nonadaptive hypothesis. Contrasting predictions of the bond-testing and alliance-formation hypothesis are presented for future testing. Copyright 1999 The Association for the Study of Animal Behaviour.     

Allonursing in Captive Guanacos,Lama guanicoe: Milk Theft or Misdirected Parental Care?

Females in several ungulates transfer milk to non-filial (NF) offspring, in a process known as allonursing. This behavior is less common in monotocous species, including most ungulates, and it has been associated with parasitic behavior of calves or mothers who have lost their own offspring. To examine whether the calves 'steal' milk from the females or whether females fail to discriminate their own calves in guanacos, allonursing behavior was observed. If milk theft drives allonursing, mothers should reject NF offspring, they should search for their own calves, and calves attempting to suckle from alien mothers should adopt parallel (as opposed to the anti-parallel) position during allonursing. Alternatively, if allonursing is caused by mothers unable to discriminate own offspring, mothers are not expected to reject NF offspring, and alien calves should use parallel and antiparallel position similarly when allonursing. Allonursing was investigated during the first 3 mo of lactation in two groups of captive guanacos composed of 15 and 14 mother-calf pairs, respectively. While 40% and 62.5% of mothers in groups 1 and 2 performed allonursing, high individual variation prevailed; some females exhibited this behavior infrequently (4.1% and 6.5 % in groups 1 and 2). The rejection rate to NF nursing attempts was threefold higher than the rejection rate to filial nursing attempts. The occurrence of nursing to NF was associated to a parallel posture by the calves. Our findings suggest that 'milk theft' is a more plausible hypothesis to explain allonursing in guanacos than 'misdirected parental care'.     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

Spatial Association in a Highly Inbred Ungulate Population: Evidence of Fine-Scale Kin Recognition

We present the first evidence of fine-scale kin recognition, based on a continuous measure of relatedness, in ungulates. The spatial association between herdmates of a captive population of aoudad ( Ammotragus lervia ), where all the individuals are related, is analysed during resting time. Our goal was to estimate which factors influence individuals' associations. The study population is highly inbred, although it does not show serious deleterious effects caused by consanguinity. It comprises a single captive herd, reproducing freely and in good conditions for more than 10 yr. It emerges that kin, measured as the coefficient of relationship between two given herdmates, is the main factor determining the spatial association (e.g. average distance) of male–male and female–female dyads, as more-related individuals tend to rest closer to each other than less-related ones. As for male–female dyads, individuals of a similar age tend to stay closer. To rule out any familiarity confounding effects, individuals' cohabitation time in the herd was added as a random factor in the analyses. Concerning the type of dyad, mother–calf dyads are characterized by higher proximity than others, particularly during the suckling period, whereas males tend to stay closer to each other than females or male–female dyads, being also more kin-related. Female social rank does not influence spatial association between herdmates. These results are related to group composition of the species in the wild, which are characterized by intense mother–calf bonds and all-male groups that are probably kin-related. It is seen that adult male–female associations are not related to kinship, but to age similarity, which is in accord with the assumption that main family groups in the wild are formed by matrilineal lines, whereas males are the dispersing sex.     

Correlated pay-offs are key to cooperation

The general belief that cooperation and altruism in social groups result primarily from kin selection has recently been challenged, not least because results from cooperatively breeding insects and vertebrates have shown that groups may be composed mainly of non-relatives. This allows testing predictions of reciprocity theory without the confounding effect of relatedness. Here, we review complementary and alternative evolutionary mechanisms to kin selection theory and provide empirical examples of cooperative behaviour among unrelated individuals in a wide range of taxa. In particular, we focus on the different forms of reciprocity and on their underlying decision rules, asking about evolutionary stability, the conditions selecting for reciprocity and the factors constraining reciprocal cooperation. We find that neither the cognitive requirements of reciprocal cooperation nor the often sequential nature of interactions are insuperable stumbling blocks for the evolution of reciprocity. We argue that simple decision rules such as ‘help anyone if helped by someone’ should get more attention in future research, because empirical studies show that animals apply such rules, and theoretical models find that they can create stable levels of cooperation under a wide range of conditions. Owing to its simplicity, behaviour based on such a heuristic may in fact be ubiquitous. Finally, we argue that the evolution of exchange and trading of service and commodities among social partners needs greater scientific focus.     

Strong reciprocity and human sociality

Human groups maintain a high level of sociality despite a low level of relatedness among group members. This paper reviews the evidence for an empirically identifiable form of prosocial behavior in humans, which we call "strong reciprocity", that may in part explain human sociality. A strong reciprocator is predisposed to cooperate with others and punish non-cooperators, even when this behavior cannot be justified in terms of extended kinship or reciprocal altruism. We present a simple model, stylized but plausible, of the evolutionary emergence of strong reciprocity.     

A case of adoption and allonursing in captive plains zebra (Equus burchellii)

Although allonursing (allowing non-filial offspring to suckle) can be a costly behaviour, it has been reported for many mammals including ungulate species. However, such behaviour is very rare in equids. This is the first report on adoption and allonursing in captive plains zebra (Equus burchellii), recorded in the Dv?r Králové Zoo, Czech Republic. We observed a case of adoption of an orphaned foal by a lactating mare, who then regularly nursed two foals (filial and non-filial). The allonursing mare rejected more suckling attempts, terminated suckling bouts more often, and had a shorter suckling bout duration than other mares. When nursing both foals at the same time, the suckling bout lasted for less time than when nursing a single foal, regardless of whether it was filial or non-filial. The allonursing mare apparently did not discriminate between the filial and non-filial foal.     

Food transfers in capuchin monkeys: an experiment on partner choice

Although most primates live in groups, experiments on reciprocity usually test individuals in dyads. This could hide the processes emerging in richer social settings, reducing the ecological validity of the results. We run an experiment on reciprocal food transfers testing capuchin monkeys (Cebus apella) in triads, so that subjects could choose to allow access to their food to either of their two partners. We tested the hypothesis that partner choice was related to a comparison of long-term social bonds with the two partners, more than to a comparison of recent food transfer events from the two partners. The results confirmed this hypothesis, thus supporting the notion that reciprocal partner preferences are based on long-term accounts of benefits that have been exchanged.     

Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons

In a mixed-sex, captive group of hamadryas baboons (Papio hamadryas hamadryas) we investigated whether female grooming relationships are affected by their dominance ranks. Seyfarth's [1977] grooming for support model and Barrett et al.'s [1999] biological market model both predict that in primate groups where competition for monopolizable resources is high, grooming among females is based, at least partly, on the interchange of grooming for rank-related benefits, and that rank thus influences the distribution of grooming in females. Contrary to this prediction, our results show that despite the existence of a linear dominance hierarchy, rather strict dominance relationships, and high food-related aggression rates, grooming among female hamadryas baboons is not affected by rank and is only exchanged for itself. This is understandable since rank differences in our study group only result in differential access to limited, preferred food items that are not actively shared. Although some females are more likely to tolerate one another at the food pile, this tolerance is not determined by their grooming efforts and interchange of grooming for rank-related benefits does not occur. We conclude that female hamadryas baboons groom others in order to be groomed by them, which is supported by our observation that grooming reciprocity within a dyad increases when more grooming occurs in this dyad. Our results indicate that grooming is indeed a valuable commodity in itself, probably because of its stress- and tension-reducing effect. Based on our findings, the existing groom trade model is extended to include circumstances in which monopolizable resources are available but are not traded for grooming.