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Allomothering in a captive colony of Hanuman langurs (Presbytis entellus)
(Presbytis entellus) Patricia A. Scollay and Patricia DeBold San Diego State University
Quantitative data on infants in a stable troop of Hanuman langurs (Presbyfis entellus) at the San Diego Zoo were collected to determine the identity and competence of their allomothers. Most allomothering (67.1%) was directed at infants less than three months old and 53.6% of it was done by juvenile females. Yearling females and juvenile males were gentle, solicitous allomothers, whereas older juvenile and adult females were often rough and inconsistent in their treatment of infants. The prevalence of juvenile allomothers suggests that allomothering did not evolve because of its adaptive value to mothers and infants, and the apparent lack of improvement in the skills of juvenile allomothers casts doubt on the theory that allomothering is adaptive as a learning experience for allomothers. Thus allomothering may not have adaptive value of its own, but rather may have evolved as part of a total behavioral complex. Key Words:
Allomothering; Langurs.
INTRODUCTION
In recent years, researchers interested in the social development of young animals have broadened the scope of their investigations to include interactions with other conspecifics, as well as those with the mother. The phenomenon of allomothering, referred to variously as aunting, infant transfer, babysitting, or play mothering-that is, the care of infants by individuals other than the mother-has received particular
ReceivedJune 30, 1980; revised October 1. 1980. Address reprint requests to: Dr. Patricia Scollay, Department of Anthropology, San Diego State University, San Diego, CA 92182, USA.
attention. Impetus for this stems from two important sources. First is the increased amount of data from species, notably the colobine and cercopithecus groups, in which the mothers and infants enjoy a less exclusive relationship than the more traditionally studied macaque and baboon group. The second source is the increasing use of sociobiological theory as a point of departure for discussions of the evolution of behavior. Allomothering is an interesting sociobiological phenomenon because it involves investment in the perpetuation of another’s genes. Allomothering has been described in a number of genera, including macaques (Hinde and Spencer-Booth, 1967), vervets (Krige and Lucas, 1974; Lancaster, 1971; Struhsaker, 1967), langurs (Hrdy, 1977; Jay, 1962; Poirier, 1968; Sugiyama, 1965, 1967), and squirrel monkeys (DuMond, 1968; Rosenblum, 1971). These descriptions are largely anecdotal in nature. Although they are frequently cited in theoretical discussions of allomothering (cf. Hrdy, 1976: Quiatt, 1979), they provide insufficient data to adequately support any theoretical stance. From a theoretical standpoint, allomothering is usually assumed to be adaptive and is discussed in terms of the relative benefits and risks to each of the individuals involved (McKenna, 1979). Such discussions are not conclusive but do have the heuristic potential of generating hypotheses that can be tested with quantified data from an intensive study of allomothering. For example, several authors have suggested that allomothering is adaptive to mothers and infants because it frees the mother for foraging (Hrdy, 1976; Poirier, 1968), provides potential adopting mothers (Hrdy, 1976; Krige and Lucas, 291
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P. A. Scollay and P. DCBold
292 1974), or aids in the socialization of the infant, perhaps by conferring a higher status on the infant because the allomother is dominant to the mother (Hrdy, 1976; Krige and Lucas, 1974). For these benefits to outweigh the potential risks to the infant, the allomother must be almost as competent as the mother and, in the later case, dominant to her. Moreover, the benefits would be greater for older infants because small infants are less cumbersome for the mother to carry and probably less apt to benefit from exposure to more dominant animals. It has also been suggested that allomothering benefits the mother and infant by providing a pool of potential adoptive mothers. For a young infant, successful adoption is only possible if the adopting mother is capable of lactating and has no infant of her own to compete for the nipple. Thus, assuming that the major adaptive value of allomothering lies with the mother and infant, the following hypothesis is generated: the allomother will be an adult, multiparous female without a nutritionally dependent infant of her own and the infant being allomothered will probably be older and less vulnerable. Allomothering will benefit the allomother, on the other hand, if it provides necessary training in infant care (Hrdy, 1976; Krige and Lucas, 1974; Lancaster, 1971; Quiatt, 1979). Allomothers, in this case, should be nulliparous, perhaps juvenile, females, for, as a learning experience, allomothering would be ofjittle value to females who had already successfully raised infants. As they matured and gained experience, the skills of allomothers should improve and infants should be more comfortable and be retrieved from them less (Jay, 1965). The most valuable learning experience for allomothers would occur, of course, with young infants. Similarly allomothering associated with agonistic buffering (Deag and Crook, 1971) would benefit the allomother most when the infant is very young and the allomother either subordinate or juvenile or both. Thus, assuming that the major adaptive value of allomothering lies with the allomother generates the following hypothesis: the infants will be young and vulnerable and the allomothers themselves will be young and inexperienced. Clearly, the conditions under which allomothering is of adaptive value to the mother and infant cannot occur simultaneously with those in which maximum benefits accrue to the allomother. More recently Quiatt (1979) proposed an-
other possibility: “allomaternal behavior may be no more than a fortuitous outcome of selection for a behavioral orientation toward young conspecifics.” The care of another’s infant is seen by him as an extension of caretaking behavior that has evolved and been selected for by the necessity of caring for one’s own infant. This theoretical stance implies that all troop members, or at least all females, would exhibit an interest in infants, particularly young infants. The form and frequency of allomothering, however, might be highly variable because there is no strong selective force acting on the behavior pattern to reduce individual variability. Another hypothesis is generated: all females will attempt to allomother infants, particularly young infants, but the frequency and form of the behavior will be highly variable among individuals. Testing these hypotheses requires data on the identity, competence, and relative contributions to the care of the infant of each allomother. The purpose of this paper is to present quantified data on allomaternal behavior in Hanuman langurs (Presbytis entellus), a species for which the occurrence of this behavior in nature has been well documented (Hrdy, 1977; Jay, 1962, 1965; Sugiyama, 1965, 1967) but not quantified for recognizable individuals. These data can then be used to test the hypotheses generated by sociobiological theory.
METHOD
The subjects were infants born into a colony of Hanuman langurs, housed in a large outdoor facility in an area of the San Diego Zoo that was inaccessible to the public. The domed, wiremesh enclosure was 10 meters in diameter with wood platforms and bars at various levels to provide the langurs with access to 10 meters of vertical space. Adjacent to the enclosure were three small cement block bedrooms that were heated in cold weather and were always available to the animals, but never to the observers. The enclosure was cleaned daily and the animals were fed a diet of monkey chow, vegetables, and browse each day but they were free of human interference at all other times. Behavioral observations were recorded from outside the enclosure. Sixteen infants, eight of which were male, were born in the colony where they lived with
Allomothering
in Hanuman
293
Langurs
number of individuals observed for each of the ten months therefore varies from two to six (see Fig. 1). Observations were taken using the focal animal method (Altmann, 1974). The behavior of the focal animals was recorded on a standardized data sheet for 15 minutes, after which a second focal animal was used. The order of focal animals was predetermined and the initial position changed daily to ensure that all individuals were observed equally during all parts of the observation session. The first 10 minutes of each observation were devoted to recording the frequencies of social interactions with all other group members on a frequency checklist. The behavior of the focal animal at the beginning of the observation session was scored; thereafter, a score was recorded only at the onset of a new behavior. Thus, to receive a frequency score greater than unity for a given behavior, a animal must have interrupted the behavior with another behavior and then returned to the first behavior during the same observation session. Duration of play and maternal contact were recorded, using a stopwatch, during the remaining 5 minutes. The data from each focal animal were partitioned by age in months and data were summed
their mothers for various lengths of time. They were part of a social group that has varied in size from 12 to 20 animals since its formation in 1972. It typically contains one adult male, between four and seven adult females, and an assortment of young langurs of both sexes. Although animals occasionally leave the colony because of death or transfers to other institutions, no new animals have entered the group, save the infants born into it. The group has, thus, been a stable social unit for many years. Systematic observations on all juveniles in the group have been collected for live years to provide longitudinal developmental data. Although there were rarely more than two animals in any age class at any point in time, it was possible to increase the number of subjects in most cases by summing data for several years. Thus, for example, data for several two-month-old infants were combined, although they were not two months old at the same time. The data presented here were collected on 13 individuals, 6 of them males, during the first 10 months of life. Unfortunately, five of the male infants did not survive their first year of life and other infants were removed from the colony. In addition, during some months of each year observations could not be taken regularly because the animals retreat to the bedrooms in the rain. The total
AGE OF INFANT (MO.%) MIN. OF OBSERVATION NUMBER OF SUBJECTS
Figure 1.
1
i
3
4
5
6
760
1180
1320
280
580
870
4563445423
Mean rates of infant care by month.
7 700
8
9
lb
860
280
620
294
across subjects of the same age. The allomothering data presented here represent 117.5 hours during which behavior was recorded on the frequency checklist portion of the data sheets of focal animals less than 11 months of age. Only the frequencies of behavior that could be unambiguously defined as infant care are considered here. These include ventral contact, hugs, being carried either ventrally or dorsally, nursing. Grooming is not included because it was difficult to distinguish grooming that was strictly care of the infant from grooming that was a more mature form of social interaction. An additional 55 hours of data were collected on the allomothering of infants less than one month old, in which allomothering was defined as ventral contact. The identity of the allomother as well as the duration of the hold were recorded. Six infants were used as focal animals for this portion of the study and each was observed on at least five occasions, spaced several days apart, during its first month of life. For 35 of these hours, both successful and unsuccessful attempts to allomother were scored; successes were those in which the prospective allomother gained control of the infant. All other attempts were scored as unsuccessful. A space for recording data on the form of allomothering and the response of the infant to the allomothering experience was available on the bottom of each of the data sheets used in the collection of quantitative data. No attempt was made to quantify these data, which were recorded ad libidum (Altmann, 1974). They did, however, form the basis of descriptions of the form of allomothering and of the determinations of the skill of the allomother.
P. A. Scollay and P. DeBold was more gradual after the third month. Allomothering, on the other hand, remained constant during the first two months, declined rapidly for the next two months, and thereafter was relatively stable. In fact, 67.1% of the observed allomothering occurred in the first two months, while only 30.2% of maternal care occurred during the same period. Infants were cared for by virtually all members of the group, although most frequently by juvenile females. Of the 608 recorded bouts for which the allomother was identified, 53.6% involved juvenile females (see Table l), who played a particularly important role during the first two months of the infants’ lives. Although there were usually more adult than juvenile females, they contributed only 35.2% of the total allomothering. Males cared for infants much less frequently. While juvenile males were responsible for 10.5% of the allomothering, the adult male was observed holding an infant only four times. The females in this colony began allomothering when they were as young as three months old. They typically carried neonatal infants on their ventrums while attempting to evade older
Table 1. Mean Rates of Allomaternal (Per Minute) Age of
Age/Sex
Class
of
Care
Allomother
Infant
Adult
Juvenile
Adult
(month)
Female
Female
Male
0.095 (4.00)” 0.068 (3.80) 0.050 (4.00) 0.021 (4.67) 0.007 (4.50) 0.024 (5.00) 0.009 (4.80) 0.021 (3.80) 0.014 (5.00) 0.006 (5.00)
0.330 (3.25) 0.154 (3.40) 0.032 (3.33) 0.042 (3.00) 0.021 (3.00) 0.021 (2.00) 0.0 (2.20) 0.00 (2.00) 0.000 (1.00) 0.010 (I .67)
0.005 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000
1 2 3
RESULTS
4
During the first ten months of life, the infants received care at a mean rate of 0.283 instances per minute. Of the 1996 recorded bouts of infant care, 60.8% involved the mother; the others were instances of allomothering. Care was not distributed equally throughout the first ten months of the infant’s life but was concentrated in the early months (see Fig. 1). Over 20% occurred in the first month alone. Total care dropped off rapidly until the third month and declined more slowly throughout the next seven months. The declins of maternal care paralleled that of total care, although its decline
5 6 7 8 9 10 ” Numbers
in parentheses
animals in the age/sex of that age.
(1.OO) 0.000 (1.00) 0.000 (1.00)
Juvenile Male 0.020 (2.75) 0.017 (2.60) 0.028 (2.67) 0.000 (3.00) 0.003 (3.00) 0.006 (3.00) 0.015 (3.00) 0.006 (3 .OO) 0.000 (3.00) 0.003 (3.00)
are the means of the number of class which were available to infants
Allomothering
in Hanuman
Langurs
females intent upon taking the infant from them. Being very close in size to their young allomothers, the neonates vocalized loudly as their backs were dragged along the cement. However, by the time these infant allomothers reached seven or eight months of age, they were highly successful at providing sufficient comfort so that their small charges rarely vocalized. They had also become quite adept at evading the older females who tried to remove the neonate from them. Yearling females were the most skillful aunts. Older juveniles, as well as adults, usually held the infants in awkward positions: upside down, under their feet while pulling on the infant’s limbs with their hands, balanced precariously on their head or shoulders, or even under a leg. One two-year-old, who had been highly competent as a yearling, developed the habit of carrying infants in her mouth. Thus, in general, the allomothering experience was not one of comfort for the infant. The initiation of allomothering was likewise potentially uncomfortable for the infant. A potential allomother usually placed an arm around the infant’s back in her attempt to take it, but it was by no means rare to observe her simply grab an arm or leg and pull. Sometimes the animal holding the infant relinquished it immediately but often she held the other arm firmly, making the infant, in effect, the object of a tug-of-war. Although allomothering often appeared abusive, infants were never hurt during any of these maneuvers. They did, however, vocalize loudly, which only rarely brought their mothers to retrieve them. Most often the mothers did not respond to their screeches in any observable fashion. Mothers and yearling aunts were rarely observed handling infants in this slightly abusive manner. They usually held the infants ventrally, occasionally grooming them, although mothers of very young infants were observed holding them upside down to examine their genitals. Males rarely acted as allomothers, but when they did, the infants were held or carried ventrally. The allomothering ofjuvenile males, thus, resembled the care given by very young female aunts or mothers rather than that given by female allomothers of their own age. Because so much allomothering occurred in the first month of the infant’s life, an intensive 55-hour study of this period was conducted on six infants. For this study, infant care was op-
295 erationally defined as ventral contact. Ten hours of observation were taken during the midday rest period, while the remainder of the observations were made at various times throughout the day when the animals were more active. Because the patterns of allomothering were strikingly different during the rest periods, those data will be considered separately. During the rest periods, infants spent 70.7% of their time in ventral contact with their mothers. Whennot resting with their mothers, infants were usually with juvenile and yearling aunts, 27.2% of the total time, and were with adult aunts more rarely, only 2.2% of the time. Moreover the infants were in continual contact with an older monkey during these periods and were never observed playing or exploring on their own. At other times during the day, when the group was more active, infants were much more independent. They were held a mean of only 81.8% of the time they were observed. Mothers accounted for a much lower percentage of the time held, 41.4%, when the group was more active. Infants were held by juvenile and yearling aunts even more than by their mothers, 47.1% of the time, which was 61.2% of the allomothering. The mean percent of total time held, as well as the mean percent of the frequency of holds and the mean length of holds, are presented in Table 2. In spite of considerable individual variation, the pattern of the infants’ care was remarkably constant, i.e., most of the care was provided by juvenile aunts and the least by adult aunts, with mothers intermediate. A Friedman two-way analysis of variance of the total time each infant was held by juvenile aunts, mother, and adult aunts showed this pattern to be statistically significant (Xz = 10, p < 0.01). Juvenile females were not only allomothers of infants in their first month more frequently than their adult counterparts, but their holds lasted longer as well. Of the juvenile female allomothers, those less than 18 months old merit special mention. Although they represented only 12.9% of the available allomothers, they accounted for 16.0% of the total time the infants were with allomothers. Moreover, the mean length of their holds was 3.84 minutes, slightly longer than the mean of 3.58 minutes for older juveniles. Thus, in spite of their youth, very young females contributed to the care of infants in a significant way.
P. A. Scollay and P. DeBold
296 Table 2. Ventral Holds of One Month Old Infants
Age/Sex Class
Proportion of Total Group
Mothers
0.086
Adult females
0.242
Juvenile females
0.348
Over I8 months Less than I8 months Juvenile males
0.227 0.121 0.212
Adult males
0.080
Proportion of Total Proportion of Total Number of Holds Time Held (Range) (Range) 0.230 (0.106-0.342) 0.224 (0.068-0.473) 0.540 (0.373-0.645) 0.460 0.080 0.006 (0.000-0.023) 0.000
However, although they spent considerable time allomothering and appeared to be more proficient than older allomothers, yearling allomothers were the least successful of all females in their attempts to take these very young infants from other allomothers. Expressing successful attempts as a percentage of total attempts, yearling aunts had a success rate of only 37.8%. Compared to this, adult females were successful 58.8% of the time and older juvenile females were the most successful, with a success rate of 69.9%. The percentage of successful attempts at retrieving their infants was highly variable among mothers, ranging from 100% to 45.5% with a mean of 79.2%. Interestingly, there was no correlation between the dominance position or the previous maternal experience of the mothers and their rate of successful retrieval rate. The mother who was least successful was intermediate in dominance, as was the mother who was most successful. In addition they were within five months of the same age. The former had three surviving offspring in the group, the latter had two, and both had been adopted and simultaneously raised by the same adult female when they were infants. In fact, there was considerable individual variability in general in the behavior of both mothers and allomothers. For example, although the mean length of holds for adult females was 1.8 minutes, the range of individual means was from 20 seconds to 10.1 minutes. For mothers the range was from 4.2 to 10.1 minutes, while the mean was 8.1 minutes. This range of variability was particularly striking from the standpoint of the experiences of individual infants. At one extreme was an infant who spent only 12.9% of its
0.414 (0.129-0.667) 0.114 (0.028-0.281) 0.471 (0.333-0.602) 0.375 0.096 0.001 (0.000-0.002) 0.000
Mean Length of Holds (Minutes) (Range) 8.09 (4.20-10.08) I .80 (0.3-10.08) 3.75 (0.17-13.02) 3.58 3.84 0.42 (0.08-0.76) 0.000
time with its mother, 9.1% with adult aunts, and 78.0% with juvenile allomothers. Another infant, at the other extreme, spent 66.7% of its time with its mother, 2.8% with adult aunts, and 31.5% with juvenile aunts.
DISCUSSION Allomothering in this captive troop was such a pervasive behavior pattern that one cannot deny the profound part it must play in the developmental experiences of infant Hanuman langurs. Soon after birth, infants’ transfers began with no resistance from the mother, which is consistent with field reports on this species (Hrdy, 1976; Jay, 1962, 1963, 1965; Sugiyama, 1965, 1967). Although infants received most of their care from their mothers, it is worthy of note that, at least in the first month of their lives, infants spent the majority of their waking hours (58.6%) in the care of allomothers. After the second month, allomothering decreased, which was a few weeks later than reported for langurs in the field (Sugiyama, 1965). Contact with conspecifits other than the mother, however, did not decrease because allomothering was replaced, not by increased maternal care, but by peer interactions. Thus the social influence of conspecifits, other than the mother, remained great throughout infancy. It is, therefore, not surprising to find many authors who have assumed that such a pervasive behavior pattern must have specific adaptive value. However, the data presented here do not confirm the hypotheses that were generated by theoretically assigning the major adaptive value either to infants and mothers or to allomothers.
Allomothering
in Hanuman
Langurs
It was hypothesized that allomothers would be older and competent and that infants, too, would be older and less vulnerable, if the major adaptive value of allomothering was for mothers and infants. Clearly this was not the case. Juvenile females were responsible for 53.6% of all allomothering, and 67.1% of all allomothering involved infants less than three months old. The presence of an adopting mother would be of critical importance to a needy infant, and it seems likely that a species which engages frequently in allomothering would be more inclined to adopt orphaned infants. However, the allomothering experience does not provide the infant with the opportunity to form a bond with a particular female who might be a potential adopting mother. When infants were so young that lactation was a limiting factor to the success of an adoption, they were being allomothered almost exclusively by juvenile females. The preponderance of juvenile allomothers likewise negates the hypothesis that adaptiveness to the infant is attributed to increased social contacts. The great range of social contacts and diverse social experiences to which infant langurs are exposed as a result of allomothering is undeniable. However, a juvenile allomother is not likely to be dominant to the infant’s own mother. Moreover, dominance in this species, at least among the females, has been shown to be related to reproductive value rather than to kin or other social relationships (Hrdy and Hrdy, 1976), and the relationship between dominance and reproductive success is at present unclear (cf. Hausfater, 1975). Thus, although the broadening of an infant’s social base by the experience of allomothering may be a profound developmental influence, it is difficult to imagine how it increases the infant’s future reproductive success. It has been suggested that aunting is adaptive for the mother because it frees her to forage unencumbered (Hrdy, 1976; Poirier, 1968). While foraging is not an important consideration in the captive environment, it is interesting to note that the times of the day during which the group would be most apt to forage, the morning and late afternoon (Jay, 1965), are the hours of the day when allomothering occurs most frequently. However, the infants most frequently allomothered were not older infants, who might have seriously encumbered their mother’s foraging. They were, instead, infants less than three
297 months old who would have been too small to be more than a minor inconvenience to their mothers. In the search for the adaptiveness of allomothering, then, we must look elsewhere. The second proposition was that allomothering was of major adaptive value to the allomother, either because it afforded the necessary training in infant care or because of advantages conferred as a result of agonistic buffering. This implies that the allomothers would be young, as would the infants, which was certainly the case in this colony. Allomothering undoubtedly provides an opportunity to learn the skills necessary to ensure the survival of potential offspring, as Lancaster (1971) and others have suggested. Furthermore, most allomothering was done by juveniles, which is consistent with the findings of others (Hrdy, 1974; Lancaster, 1971; SpencerBooth, 1968; Zucker, 1978). However, because young langurs seem to learn appropriate maternal behaviors very rapidly and are quite competent by the time they are yearlings, this may have less adaptive significance than was previously thought. It is unlikely that further learning occurs after the initial exposure to infants because, by the time they are two years old, juvenile females have adopted the inefticient form of allomothering observed in adults. Furthermore, there seems to be a rather wide variety of maternal behavior that is sufficient to ensure the survival and adequate socialization of infants rather than one narrowly circumscribed pattern. One must, therefore, at least question the adaptiveness of the learning experience to those individuals who are providing most of the allomothering, that is, the juvenile females over two years old. The classic form of agonistic buffering described by Deag and Crook (1971) was rarely observed in this colony. Juvenile males never carried infants when they approached the dominant male and very rarely carried one when being chased by him. It seems unlikely that the allomothering of juvenile males was related to agonistic buffering; for, if it was, the form was so subtle that it was used to prevent aggression by the adult male who was sitting in a distant part of the enclosure engaged in his own pursuits. Since a strong adaptive advantage to any of the individuals involved in allomothering cannot be supported by these data, Quiatt’s (1979) suggestion-i.e., allomothering is selected for pri-
298 marily as part of a general pattern of interest in infants rather than because of some special adaptive value to one of the parties involved-is particularly appealing. Moreover, the variability in both allomaternal behaviors and the amount of allomothering to which an infant is exposed strengthens that argument. Such variability implies that there is no strong selective force acting on that behavior. The question arises whether data on captive animals can be used to evaluate the adaptiveness of a behavior pattern. To answer that question, we must compare these data with those from field reports. Although the general form, pervasiveness and time of onset of allomothering in this colony was remarkably similar to that described in field studies (Hrdy, 1976; Jay, 1962, 1963, 1965; Sugiyama, 1965, 1967), there appear to be some important differences in the quality of that care. Jay (1965) measured the skill of the female by the length of time she could hold an infant before it squirmed and squealed. She observed that there was considerable variation among females in their skill, but that few were clumsy or awkward. While few of the females in this colony were clumsy or awkward with their own infants, they were almost universally clumsy and awkward with the infants of others. Other reports of clumsy handling have been attributed to lack of experience (Hrdy, 1976), but such was definitely not the case in this study, for it was the yearling allomothers who handled the infants with the greatest skill. Jay (1965) further suggested a positive correlation between the amount of previous maternal experience and the efficiency of handling infants, though it is unclear whether this statement is restricted to the care given by mothers to their own infants. These data, however, suggest that if there is a correlation between maternal experience and allomaternal skill, it is negative. Multiparous females were less often allomothers and were less skillful than their juvenile counterparts, although they were more successful in their attempts to allomother. In addition, the subjects of this study responded rather differently to the obvious distress of the infant. Jay (1965) reported that newborns were taken by another female at the first sign of discomfort. Our infants frequently vocalized for extended periods without being rescued by another female. Mothers rarely responded to their vocalizations, and when they did, the mean success rate of their attempted
retrievals was only 79.2%, with a range of from 45.5% to 100%. They were, however, equally successful in retrievals from juveniles and dominant females. For some mothers, at least, this was strikingly different from Jay’s report that the mother &‘can take her infant from any female in the troop...” Thus, it is apparent that, while the general pattern of allomothering described here is similar to description for this species in nature, the details differ somewhat. It is difficult to ascertain the sources of these differences, particularly in light of the general lack of precision in field descriptions. Undoubtedly the safety of the captive environment allows a wider range of variability in the form of this particular behavior pattern. However, the extent to which the pattern is species-specific, and therefore biologically entrained, could not be greatly altered in only one generation of captivity. It seems logical to assume, therefore, that the more precise quantification and the closer observation that is possible in the captive situation has allowed the range of variation of these behaviors to be described more accurately. This raises the interesting possibility that hypotheses concerning the adaptive value of allomothering can be tested more adequately with precise quantitative data from captive animals than with descriptions from field studies that are unavoidably incomplete and imprecise. Based on its pervasiveness alone, one must conclude that allomothering is important to the development of infant langurs. This, however, need not imply that by itself allomothering has specific adaptive value to any of the individuals involved. Based on these data, we can only conclude, like Quiatt (1979), that allomothering is an extension of a general adaptation to provide adequate care for one’s own infant, which may be fortuitous, but was not selected for per se. This study does point to two important considerations for those engaged in theoretical discussions of the adaptive value of particular behavior patterns: (1) that precise and quantitative descriptions of the behavior pattern must precede any valid theoretical discussion of its adaptive value, and (2) that even very pervasive behavior patterns may not have adaptive value in and of themselves, but rather may have been selected for as part of a total behavioral complex. We would like to express our appreciation to the staff of the San Diego Zoo and the San Diego Zoological
299
Society for their assistance over the years of this study. Special thanks to John Bartlett, Cheryl Borges, Peggy Erin, Fred Kidder, Tricia McNamara, Peter Mobley, Ed Powers, Chris Sibley, and the other San Diego State University students who have expressed their interest in Hanuman langurs by spending hours observing them. We are very grateful to the late Christopher Parker and to Sue Archer for assistance with computer programs and particularly thankful for the valuable contributions Dr. Marilyn Borges and Dr. Joseph Levine made to the manuscript. This research was funded, in part, by a San Diego State University Faculty Grantin-Aid to P.A. Scollay.
Jay, P. Aspects of maternal behavior among langurs. Ann. N.Y. Acad. Sci. 102: 468-476 -.
Sci. 2: 55-61 (1974).
Lancaster, J. Play-mothering: The relations between juvenile females and young infants among freeranging vervet monkeys (Cercopithecus aethiops). Folia Primat.
REFERENCES Altmann, J. Observational study of behavior: Sampling methods, Behaviour, 49: 227-267 (1974). Deag, J.M., Crook, J.H. Social behavior and agonistic buffering in the wild barbary macaque Mucara sylvanus. Folia Primat. 15: 183-200 (1971). DuMond, F.V. The squirrel monkey in a seminatural environment. In The squirrel monkey, L.A. Rosenblum & R.W. Cooper (Eds.). New York: Academic Press, 1968, pp. 87-145. Hausfater, G. Dominance and reproduction in baboons (Papio cynocephalus): A quantitative analysis. Contrib. Prim&o/. 7. Hinde, R.A., Spencer-Booth, Y. The effect of social companions on mother-infant relations in rhesus monkeys. In Primate Ethology, D. Morris (Ed.). Chicago: Aldine, 1967, pp. 267-286. Hrdy, S.B. Male-male competition and infanticide among the langurs (Presbytis enrellus) of Abu’ Rayasthan. Folia Primat. 22: 19-58 (1974). -. Care and exploitation of nonhuman primate infants by conspecitics other than the mother. Ad-.
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vance. Stud. Behav. 6: 101-158 (1976). The langurs of Abu. Cambridge: Harvard Uni-
versity Press, 1977. Hrdy, D.B. Hierarchical relations among female hanuman langurs (Primates: Colobinae, Presbytis entellus). Science 193(4256): 913-915 (1976).
(1962).
relations in langurs. In Maternal behavior in mammals, H. Rheingold (Ed.). New York: Wiley, 1963, pp. 282-304. -. The common langur of North India. In Primate behavior, I. DeVore (ed.). New York: Holt, Rinehart, & Winston, 1965, pp. 197-249. Krige, P.D., Lucas, J.W. Aunting behavior in an urban troop of Cercopithecus aethiops. J. Behav. Mother-infant
15: 161-182 (1971)
McKenna, J.J. Aspects of infant socialization, attachment, and maternal caregiving patterns among primates: A cross-disciplinary review. Yearbook of Physical Anrhropology
22: 250-286
(1979).
Poirier, F.E. Nilgiri langur (Presbyris johnii) mother infant dyad. Primates 9: 45-68 (1968). Quiatt, D. Aunts and mothers: Adaptive implications of allomaternal behavior of nonhuman primates. Amer. Anthrop.
Rosenblum,
81: 310-319
(1979).
L.A. Infant attachment
in monkeys. In R. Shaffer Press, 1971, pp.
The origins of human social relations,
(Ed.). New York: Academic 85-113. Spencer-Booth, Y. The behavior of group companions towards rhesus monkey infants. Anim. Behav. 16: 541-557
(1968).
Struhsaker, T. Behavior of vervet monkeys (Cercopithecus aethiops). University of California Publications in Zoology 82: 1-64 (1967).
Sugiyama, Y. Behavioral development and social structure in two troops of hanuman langurs (Presbytis entellus). Primates 6: 213-247 -.
(1965).
Social organization of Hanuman langurs. In Social communications among primates, S. Altmann (Ed.). Chicago: University of Chicago Press, 1967, pp. 221-236. Zucker, E. Allomaternal behavior in a group of freeranging patas monkeys. Paper presented at the annual meetings of the American Society of Primatologists, Atlanta, 1978.
Quantitative data on infants in a stable troop of Hanuman langurs (Presbyfis entellus) at the San Diego Zoo were collected to determine the identity and competence of their allomothers. Most allomothering (67.1%) was directed at infants less than three months old and 53.6% of it was done by juvenile females. Yearling females and juvenile males were gentle, solicitous allomothers, whereas older juvenile and adult females were often rough and inconsistent in their treatment of infants. The prevalence of juvenile allomothers suggests that allomothering did not evolve because of its adaptive value to mothers and infants, and the apparent lack of improvement in the skills of juvenile allomothers casts doubt on the theory that allomothering is adaptive as a learning experience for allomothers. Thus allomothering may not have adaptive value of its own, but rather may have evolved as part of a total behavioral complex. Key Words:
Allomothering; Langurs.
INTRODUCTION
In recent years, researchers interested in the social development of young animals have broadened the scope of their investigations to include interactions with other conspecifics, as well as those with the mother. The phenomenon of allomothering, referred to variously as aunting, infant transfer, babysitting, or play mothering-that is, the care of infants by individuals other than the mother-has received particular
ReceivedJune 30, 1980; revised October 1. 1980. Address reprint requests to: Dr. Patricia Scollay, Department of Anthropology, San Diego State University, San Diego, CA 92182, USA.
attention. Impetus for this stems from two important sources. First is the increased amount of data from species, notably the colobine and cercopithecus groups, in which the mothers and infants enjoy a less exclusive relationship than the more traditionally studied macaque and baboon group. The second source is the increasing use of sociobiological theory as a point of departure for discussions of the evolution of behavior. Allomothering is an interesting sociobiological phenomenon because it involves investment in the perpetuation of another’s genes. Allomothering has been described in a number of genera, including macaques (Hinde and Spencer-Booth, 1967), vervets (Krige and Lucas, 1974; Lancaster, 1971; Struhsaker, 1967), langurs (Hrdy, 1977; Jay, 1962; Poirier, 1968; Sugiyama, 1965, 1967), and squirrel monkeys (DuMond, 1968; Rosenblum, 1971). These descriptions are largely anecdotal in nature. Although they are frequently cited in theoretical discussions of allomothering (cf. Hrdy, 1976: Quiatt, 1979), they provide insufficient data to adequately support any theoretical stance. From a theoretical standpoint, allomothering is usually assumed to be adaptive and is discussed in terms of the relative benefits and risks to each of the individuals involved (McKenna, 1979). Such discussions are not conclusive but do have the heuristic potential of generating hypotheses that can be tested with quantified data from an intensive study of allomothering. For example, several authors have suggested that allomothering is adaptive to mothers and infants because it frees the mother for foraging (Hrdy, 1976; Poirier, 1968), provides potential adopting mothers (Hrdy, 1976; Krige and Lucas, 291
Ethology and Sociobiology 1: 291-299 (1980) 0 Else&x North Holland, Inc., 1980 52Vanderbilt Ave., New York, New York 10017
0162-3095/80/040291-09$02.25
P. A. Scollay and P. DCBold
292 1974), or aids in the socialization of the infant, perhaps by conferring a higher status on the infant because the allomother is dominant to the mother (Hrdy, 1976; Krige and Lucas, 1974). For these benefits to outweigh the potential risks to the infant, the allomother must be almost as competent as the mother and, in the later case, dominant to her. Moreover, the benefits would be greater for older infants because small infants are less cumbersome for the mother to carry and probably less apt to benefit from exposure to more dominant animals. It has also been suggested that allomothering benefits the mother and infant by providing a pool of potential adoptive mothers. For a young infant, successful adoption is only possible if the adopting mother is capable of lactating and has no infant of her own to compete for the nipple. Thus, assuming that the major adaptive value of allomothering lies with the mother and infant, the following hypothesis is generated: the allomother will be an adult, multiparous female without a nutritionally dependent infant of her own and the infant being allomothered will probably be older and less vulnerable. Allomothering will benefit the allomother, on the other hand, if it provides necessary training in infant care (Hrdy, 1976; Krige and Lucas, 1974; Lancaster, 1971; Quiatt, 1979). Allomothers, in this case, should be nulliparous, perhaps juvenile, females, for, as a learning experience, allomothering would be ofjittle value to females who had already successfully raised infants. As they matured and gained experience, the skills of allomothers should improve and infants should be more comfortable and be retrieved from them less (Jay, 1965). The most valuable learning experience for allomothers would occur, of course, with young infants. Similarly allomothering associated with agonistic buffering (Deag and Crook, 1971) would benefit the allomother most when the infant is very young and the allomother either subordinate or juvenile or both. Thus, assuming that the major adaptive value of allomothering lies with the allomother generates the following hypothesis: the infants will be young and vulnerable and the allomothers themselves will be young and inexperienced. Clearly, the conditions under which allomothering is of adaptive value to the mother and infant cannot occur simultaneously with those in which maximum benefits accrue to the allomother. More recently Quiatt (1979) proposed an-
other possibility: “allomaternal behavior may be no more than a fortuitous outcome of selection for a behavioral orientation toward young conspecifics.” The care of another’s infant is seen by him as an extension of caretaking behavior that has evolved and been selected for by the necessity of caring for one’s own infant. This theoretical stance implies that all troop members, or at least all females, would exhibit an interest in infants, particularly young infants. The form and frequency of allomothering, however, might be highly variable because there is no strong selective force acting on the behavior pattern to reduce individual variability. Another hypothesis is generated: all females will attempt to allomother infants, particularly young infants, but the frequency and form of the behavior will be highly variable among individuals. Testing these hypotheses requires data on the identity, competence, and relative contributions to the care of the infant of each allomother. The purpose of this paper is to present quantified data on allomaternal behavior in Hanuman langurs (Presbytis entellus), a species for which the occurrence of this behavior in nature has been well documented (Hrdy, 1977; Jay, 1962, 1965; Sugiyama, 1965, 1967) but not quantified for recognizable individuals. These data can then be used to test the hypotheses generated by sociobiological theory.
METHOD
The subjects were infants born into a colony of Hanuman langurs, housed in a large outdoor facility in an area of the San Diego Zoo that was inaccessible to the public. The domed, wiremesh enclosure was 10 meters in diameter with wood platforms and bars at various levels to provide the langurs with access to 10 meters of vertical space. Adjacent to the enclosure were three small cement block bedrooms that were heated in cold weather and were always available to the animals, but never to the observers. The enclosure was cleaned daily and the animals were fed a diet of monkey chow, vegetables, and browse each day but they were free of human interference at all other times. Behavioral observations were recorded from outside the enclosure. Sixteen infants, eight of which were male, were born in the colony where they lived with
Allomothering
in Hanuman
293
Langurs
number of individuals observed for each of the ten months therefore varies from two to six (see Fig. 1). Observations were taken using the focal animal method (Altmann, 1974). The behavior of the focal animals was recorded on a standardized data sheet for 15 minutes, after which a second focal animal was used. The order of focal animals was predetermined and the initial position changed daily to ensure that all individuals were observed equally during all parts of the observation session. The first 10 minutes of each observation were devoted to recording the frequencies of social interactions with all other group members on a frequency checklist. The behavior of the focal animal at the beginning of the observation session was scored; thereafter, a score was recorded only at the onset of a new behavior. Thus, to receive a frequency score greater than unity for a given behavior, a animal must have interrupted the behavior with another behavior and then returned to the first behavior during the same observation session. Duration of play and maternal contact were recorded, using a stopwatch, during the remaining 5 minutes. The data from each focal animal were partitioned by age in months and data were summed
their mothers for various lengths of time. They were part of a social group that has varied in size from 12 to 20 animals since its formation in 1972. It typically contains one adult male, between four and seven adult females, and an assortment of young langurs of both sexes. Although animals occasionally leave the colony because of death or transfers to other institutions, no new animals have entered the group, save the infants born into it. The group has, thus, been a stable social unit for many years. Systematic observations on all juveniles in the group have been collected for live years to provide longitudinal developmental data. Although there were rarely more than two animals in any age class at any point in time, it was possible to increase the number of subjects in most cases by summing data for several years. Thus, for example, data for several two-month-old infants were combined, although they were not two months old at the same time. The data presented here were collected on 13 individuals, 6 of them males, during the first 10 months of life. Unfortunately, five of the male infants did not survive their first year of life and other infants were removed from the colony. In addition, during some months of each year observations could not be taken regularly because the animals retreat to the bedrooms in the rain. The total
AGE OF INFANT (MO.%) MIN. OF OBSERVATION NUMBER OF SUBJECTS
Figure 1.
1
i
3
4
5
6
760
1180
1320
280
580
870
4563445423
Mean rates of infant care by month.
7 700
8
9
lb
860
280
620
294
across subjects of the same age. The allomothering data presented here represent 117.5 hours during which behavior was recorded on the frequency checklist portion of the data sheets of focal animals less than 11 months of age. Only the frequencies of behavior that could be unambiguously defined as infant care are considered here. These include ventral contact, hugs, being carried either ventrally or dorsally, nursing. Grooming is not included because it was difficult to distinguish grooming that was strictly care of the infant from grooming that was a more mature form of social interaction. An additional 55 hours of data were collected on the allomothering of infants less than one month old, in which allomothering was defined as ventral contact. The identity of the allomother as well as the duration of the hold were recorded. Six infants were used as focal animals for this portion of the study and each was observed on at least five occasions, spaced several days apart, during its first month of life. For 35 of these hours, both successful and unsuccessful attempts to allomother were scored; successes were those in which the prospective allomother gained control of the infant. All other attempts were scored as unsuccessful. A space for recording data on the form of allomothering and the response of the infant to the allomothering experience was available on the bottom of each of the data sheets used in the collection of quantitative data. No attempt was made to quantify these data, which were recorded ad libidum (Altmann, 1974). They did, however, form the basis of descriptions of the form of allomothering and of the determinations of the skill of the allomother.
P. A. Scollay and P. DeBold was more gradual after the third month. Allomothering, on the other hand, remained constant during the first two months, declined rapidly for the next two months, and thereafter was relatively stable. In fact, 67.1% of the observed allomothering occurred in the first two months, while only 30.2% of maternal care occurred during the same period. Infants were cared for by virtually all members of the group, although most frequently by juvenile females. Of the 608 recorded bouts for which the allomother was identified, 53.6% involved juvenile females (see Table l), who played a particularly important role during the first two months of the infants’ lives. Although there were usually more adult than juvenile females, they contributed only 35.2% of the total allomothering. Males cared for infants much less frequently. While juvenile males were responsible for 10.5% of the allomothering, the adult male was observed holding an infant only four times. The females in this colony began allomothering when they were as young as three months old. They typically carried neonatal infants on their ventrums while attempting to evade older
Table 1. Mean Rates of Allomaternal (Per Minute) Age of
Age/Sex
Class
of
Care
Allomother
Infant
Adult
Juvenile
Adult
(month)
Female
Female
Male
0.095 (4.00)” 0.068 (3.80) 0.050 (4.00) 0.021 (4.67) 0.007 (4.50) 0.024 (5.00) 0.009 (4.80) 0.021 (3.80) 0.014 (5.00) 0.006 (5.00)
0.330 (3.25) 0.154 (3.40) 0.032 (3.33) 0.042 (3.00) 0.021 (3.00) 0.021 (2.00) 0.0 (2.20) 0.00 (2.00) 0.000 (1.00) 0.010 (I .67)
0.005 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000 (1.00) 0.000
1 2 3
RESULTS
4
During the first ten months of life, the infants received care at a mean rate of 0.283 instances per minute. Of the 1996 recorded bouts of infant care, 60.8% involved the mother; the others were instances of allomothering. Care was not distributed equally throughout the first ten months of the infant’s life but was concentrated in the early months (see Fig. 1). Over 20% occurred in the first month alone. Total care dropped off rapidly until the third month and declined more slowly throughout the next seven months. The declins of maternal care paralleled that of total care, although its decline
5 6 7 8 9 10 ” Numbers
in parentheses
animals in the age/sex of that age.
(1.OO) 0.000 (1.00) 0.000 (1.00)
Juvenile Male 0.020 (2.75) 0.017 (2.60) 0.028 (2.67) 0.000 (3.00) 0.003 (3.00) 0.006 (3.00) 0.015 (3.00) 0.006 (3 .OO) 0.000 (3.00) 0.003 (3.00)
are the means of the number of class which were available to infants
Allomothering
in Hanuman
Langurs
females intent upon taking the infant from them. Being very close in size to their young allomothers, the neonates vocalized loudly as their backs were dragged along the cement. However, by the time these infant allomothers reached seven or eight months of age, they were highly successful at providing sufficient comfort so that their small charges rarely vocalized. They had also become quite adept at evading the older females who tried to remove the neonate from them. Yearling females were the most skillful aunts. Older juveniles, as well as adults, usually held the infants in awkward positions: upside down, under their feet while pulling on the infant’s limbs with their hands, balanced precariously on their head or shoulders, or even under a leg. One two-year-old, who had been highly competent as a yearling, developed the habit of carrying infants in her mouth. Thus, in general, the allomothering experience was not one of comfort for the infant. The initiation of allomothering was likewise potentially uncomfortable for the infant. A potential allomother usually placed an arm around the infant’s back in her attempt to take it, but it was by no means rare to observe her simply grab an arm or leg and pull. Sometimes the animal holding the infant relinquished it immediately but often she held the other arm firmly, making the infant, in effect, the object of a tug-of-war. Although allomothering often appeared abusive, infants were never hurt during any of these maneuvers. They did, however, vocalize loudly, which only rarely brought their mothers to retrieve them. Most often the mothers did not respond to their screeches in any observable fashion. Mothers and yearling aunts were rarely observed handling infants in this slightly abusive manner. They usually held the infants ventrally, occasionally grooming them, although mothers of very young infants were observed holding them upside down to examine their genitals. Males rarely acted as allomothers, but when they did, the infants were held or carried ventrally. The allomothering ofjuvenile males, thus, resembled the care given by very young female aunts or mothers rather than that given by female allomothers of their own age. Because so much allomothering occurred in the first month of the infant’s life, an intensive 55-hour study of this period was conducted on six infants. For this study, infant care was op-
295 erationally defined as ventral contact. Ten hours of observation were taken during the midday rest period, while the remainder of the observations were made at various times throughout the day when the animals were more active. Because the patterns of allomothering were strikingly different during the rest periods, those data will be considered separately. During the rest periods, infants spent 70.7% of their time in ventral contact with their mothers. Whennot resting with their mothers, infants were usually with juvenile and yearling aunts, 27.2% of the total time, and were with adult aunts more rarely, only 2.2% of the time. Moreover the infants were in continual contact with an older monkey during these periods and were never observed playing or exploring on their own. At other times during the day, when the group was more active, infants were much more independent. They were held a mean of only 81.8% of the time they were observed. Mothers accounted for a much lower percentage of the time held, 41.4%, when the group was more active. Infants were held by juvenile and yearling aunts even more than by their mothers, 47.1% of the time, which was 61.2% of the allomothering. The mean percent of total time held, as well as the mean percent of the frequency of holds and the mean length of holds, are presented in Table 2. In spite of considerable individual variation, the pattern of the infants’ care was remarkably constant, i.e., most of the care was provided by juvenile aunts and the least by adult aunts, with mothers intermediate. A Friedman two-way analysis of variance of the total time each infant was held by juvenile aunts, mother, and adult aunts showed this pattern to be statistically significant (Xz = 10, p < 0.01). Juvenile females were not only allomothers of infants in their first month more frequently than their adult counterparts, but their holds lasted longer as well. Of the juvenile female allomothers, those less than 18 months old merit special mention. Although they represented only 12.9% of the available allomothers, they accounted for 16.0% of the total time the infants were with allomothers. Moreover, the mean length of their holds was 3.84 minutes, slightly longer than the mean of 3.58 minutes for older juveniles. Thus, in spite of their youth, very young females contributed to the care of infants in a significant way.
P. A. Scollay and P. DeBold
296 Table 2. Ventral Holds of One Month Old Infants
Age/Sex Class
Proportion of Total Group
Mothers
0.086
Adult females
0.242
Juvenile females
0.348
Over I8 months Less than I8 months Juvenile males
0.227 0.121 0.212
Adult males
0.080
Proportion of Total Proportion of Total Number of Holds Time Held (Range) (Range) 0.230 (0.106-0.342) 0.224 (0.068-0.473) 0.540 (0.373-0.645) 0.460 0.080 0.006 (0.000-0.023) 0.000
However, although they spent considerable time allomothering and appeared to be more proficient than older allomothers, yearling allomothers were the least successful of all females in their attempts to take these very young infants from other allomothers. Expressing successful attempts as a percentage of total attempts, yearling aunts had a success rate of only 37.8%. Compared to this, adult females were successful 58.8% of the time and older juvenile females were the most successful, with a success rate of 69.9%. The percentage of successful attempts at retrieving their infants was highly variable among mothers, ranging from 100% to 45.5% with a mean of 79.2%. Interestingly, there was no correlation between the dominance position or the previous maternal experience of the mothers and their rate of successful retrieval rate. The mother who was least successful was intermediate in dominance, as was the mother who was most successful. In addition they were within five months of the same age. The former had three surviving offspring in the group, the latter had two, and both had been adopted and simultaneously raised by the same adult female when they were infants. In fact, there was considerable individual variability in general in the behavior of both mothers and allomothers. For example, although the mean length of holds for adult females was 1.8 minutes, the range of individual means was from 20 seconds to 10.1 minutes. For mothers the range was from 4.2 to 10.1 minutes, while the mean was 8.1 minutes. This range of variability was particularly striking from the standpoint of the experiences of individual infants. At one extreme was an infant who spent only 12.9% of its
0.414 (0.129-0.667) 0.114 (0.028-0.281) 0.471 (0.333-0.602) 0.375 0.096 0.001 (0.000-0.002) 0.000
Mean Length of Holds (Minutes) (Range) 8.09 (4.20-10.08) I .80 (0.3-10.08) 3.75 (0.17-13.02) 3.58 3.84 0.42 (0.08-0.76) 0.000
time with its mother, 9.1% with adult aunts, and 78.0% with juvenile allomothers. Another infant, at the other extreme, spent 66.7% of its time with its mother, 2.8% with adult aunts, and 31.5% with juvenile aunts.
DISCUSSION Allomothering in this captive troop was such a pervasive behavior pattern that one cannot deny the profound part it must play in the developmental experiences of infant Hanuman langurs. Soon after birth, infants’ transfers began with no resistance from the mother, which is consistent with field reports on this species (Hrdy, 1976; Jay, 1962, 1963, 1965; Sugiyama, 1965, 1967). Although infants received most of their care from their mothers, it is worthy of note that, at least in the first month of their lives, infants spent the majority of their waking hours (58.6%) in the care of allomothers. After the second month, allomothering decreased, which was a few weeks later than reported for langurs in the field (Sugiyama, 1965). Contact with conspecifits other than the mother, however, did not decrease because allomothering was replaced, not by increased maternal care, but by peer interactions. Thus the social influence of conspecifits, other than the mother, remained great throughout infancy. It is, therefore, not surprising to find many authors who have assumed that such a pervasive behavior pattern must have specific adaptive value. However, the data presented here do not confirm the hypotheses that were generated by theoretically assigning the major adaptive value either to infants and mothers or to allomothers.
Allomothering
in Hanuman
Langurs
It was hypothesized that allomothers would be older and competent and that infants, too, would be older and less vulnerable, if the major adaptive value of allomothering was for mothers and infants. Clearly this was not the case. Juvenile females were responsible for 53.6% of all allomothering, and 67.1% of all allomothering involved infants less than three months old. The presence of an adopting mother would be of critical importance to a needy infant, and it seems likely that a species which engages frequently in allomothering would be more inclined to adopt orphaned infants. However, the allomothering experience does not provide the infant with the opportunity to form a bond with a particular female who might be a potential adopting mother. When infants were so young that lactation was a limiting factor to the success of an adoption, they were being allomothered almost exclusively by juvenile females. The preponderance of juvenile allomothers likewise negates the hypothesis that adaptiveness to the infant is attributed to increased social contacts. The great range of social contacts and diverse social experiences to which infant langurs are exposed as a result of allomothering is undeniable. However, a juvenile allomother is not likely to be dominant to the infant’s own mother. Moreover, dominance in this species, at least among the females, has been shown to be related to reproductive value rather than to kin or other social relationships (Hrdy and Hrdy, 1976), and the relationship between dominance and reproductive success is at present unclear (cf. Hausfater, 1975). Thus, although the broadening of an infant’s social base by the experience of allomothering may be a profound developmental influence, it is difficult to imagine how it increases the infant’s future reproductive success. It has been suggested that aunting is adaptive for the mother because it frees her to forage unencumbered (Hrdy, 1976; Poirier, 1968). While foraging is not an important consideration in the captive environment, it is interesting to note that the times of the day during which the group would be most apt to forage, the morning and late afternoon (Jay, 1965), are the hours of the day when allomothering occurs most frequently. However, the infants most frequently allomothered were not older infants, who might have seriously encumbered their mother’s foraging. They were, instead, infants less than three
297 months old who would have been too small to be more than a minor inconvenience to their mothers. In the search for the adaptiveness of allomothering, then, we must look elsewhere. The second proposition was that allomothering was of major adaptive value to the allomother, either because it afforded the necessary training in infant care or because of advantages conferred as a result of agonistic buffering. This implies that the allomothers would be young, as would the infants, which was certainly the case in this colony. Allomothering undoubtedly provides an opportunity to learn the skills necessary to ensure the survival of potential offspring, as Lancaster (1971) and others have suggested. Furthermore, most allomothering was done by juveniles, which is consistent with the findings of others (Hrdy, 1974; Lancaster, 1971; SpencerBooth, 1968; Zucker, 1978). However, because young langurs seem to learn appropriate maternal behaviors very rapidly and are quite competent by the time they are yearlings, this may have less adaptive significance than was previously thought. It is unlikely that further learning occurs after the initial exposure to infants because, by the time they are two years old, juvenile females have adopted the inefticient form of allomothering observed in adults. Furthermore, there seems to be a rather wide variety of maternal behavior that is sufficient to ensure the survival and adequate socialization of infants rather than one narrowly circumscribed pattern. One must, therefore, at least question the adaptiveness of the learning experience to those individuals who are providing most of the allomothering, that is, the juvenile females over two years old. The classic form of agonistic buffering described by Deag and Crook (1971) was rarely observed in this colony. Juvenile males never carried infants when they approached the dominant male and very rarely carried one when being chased by him. It seems unlikely that the allomothering of juvenile males was related to agonistic buffering; for, if it was, the form was so subtle that it was used to prevent aggression by the adult male who was sitting in a distant part of the enclosure engaged in his own pursuits. Since a strong adaptive advantage to any of the individuals involved in allomothering cannot be supported by these data, Quiatt’s (1979) suggestion-i.e., allomothering is selected for pri-
298 marily as part of a general pattern of interest in infants rather than because of some special adaptive value to one of the parties involved-is particularly appealing. Moreover, the variability in both allomaternal behaviors and the amount of allomothering to which an infant is exposed strengthens that argument. Such variability implies that there is no strong selective force acting on that behavior. The question arises whether data on captive animals can be used to evaluate the adaptiveness of a behavior pattern. To answer that question, we must compare these data with those from field reports. Although the general form, pervasiveness and time of onset of allomothering in this colony was remarkably similar to that described in field studies (Hrdy, 1976; Jay, 1962, 1963, 1965; Sugiyama, 1965, 1967), there appear to be some important differences in the quality of that care. Jay (1965) measured the skill of the female by the length of time she could hold an infant before it squirmed and squealed. She observed that there was considerable variation among females in their skill, but that few were clumsy or awkward. While few of the females in this colony were clumsy or awkward with their own infants, they were almost universally clumsy and awkward with the infants of others. Other reports of clumsy handling have been attributed to lack of experience (Hrdy, 1976), but such was definitely not the case in this study, for it was the yearling allomothers who handled the infants with the greatest skill. Jay (1965) further suggested a positive correlation between the amount of previous maternal experience and the efficiency of handling infants, though it is unclear whether this statement is restricted to the care given by mothers to their own infants. These data, however, suggest that if there is a correlation between maternal experience and allomaternal skill, it is negative. Multiparous females were less often allomothers and were less skillful than their juvenile counterparts, although they were more successful in their attempts to allomother. In addition, the subjects of this study responded rather differently to the obvious distress of the infant. Jay (1965) reported that newborns were taken by another female at the first sign of discomfort. Our infants frequently vocalized for extended periods without being rescued by another female. Mothers rarely responded to their vocalizations, and when they did, the mean success rate of their attempted
retrievals was only 79.2%, with a range of from 45.5% to 100%. They were, however, equally successful in retrievals from juveniles and dominant females. For some mothers, at least, this was strikingly different from Jay’s report that the mother &‘can take her infant from any female in the troop...” Thus, it is apparent that, while the general pattern of allomothering described here is similar to description for this species in nature, the details differ somewhat. It is difficult to ascertain the sources of these differences, particularly in light of the general lack of precision in field descriptions. Undoubtedly the safety of the captive environment allows a wider range of variability in the form of this particular behavior pattern. However, the extent to which the pattern is species-specific, and therefore biologically entrained, could not be greatly altered in only one generation of captivity. It seems logical to assume, therefore, that the more precise quantification and the closer observation that is possible in the captive situation has allowed the range of variation of these behaviors to be described more accurately. This raises the interesting possibility that hypotheses concerning the adaptive value of allomothering can be tested more adequately with precise quantitative data from captive animals than with descriptions from field studies that are unavoidably incomplete and imprecise. Based on its pervasiveness alone, one must conclude that allomothering is important to the development of infant langurs. This, however, need not imply that by itself allomothering has specific adaptive value to any of the individuals involved. Based on these data, we can only conclude, like Quiatt (1979), that allomothering is an extension of a general adaptation to provide adequate care for one’s own infant, which may be fortuitous, but was not selected for per se. This study does point to two important considerations for those engaged in theoretical discussions of the adaptive value of particular behavior patterns: (1) that precise and quantitative descriptions of the behavior pattern must precede any valid theoretical discussion of its adaptive value, and (2) that even very pervasive behavior patterns may not have adaptive value in and of themselves, but rather may have been selected for as part of a total behavioral complex. We would like to express our appreciation to the staff of the San Diego Zoo and the San Diego Zoological
299
Society for their assistance over the years of this study. Special thanks to John Bartlett, Cheryl Borges, Peggy Erin, Fred Kidder, Tricia McNamara, Peter Mobley, Ed Powers, Chris Sibley, and the other San Diego State University students who have expressed their interest in Hanuman langurs by spending hours observing them. We are very grateful to the late Christopher Parker and to Sue Archer for assistance with computer programs and particularly thankful for the valuable contributions Dr. Marilyn Borges and Dr. Joseph Levine made to the manuscript. This research was funded, in part, by a San Diego State University Faculty Grantin-Aid to P.A. Scollay.
Jay, P. Aspects of maternal behavior among langurs. Ann. N.Y. Acad. Sci. 102: 468-476 -.
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