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Reciprocal benefits of allomothering for female vervet monkeys
Anim. Behav., 1990, 40, 553-562
Reciprocal benefits of allomothering for female vervet monkeys L Y N N A. F A I R B A N K S
Department of Psychiatry and Biobehavioral Sciences, University of CaliJbrnia, Los Angeles, CA 90024 U.S.A.
Abstract. Allomothering, or care of the young by individuals other than the mother, was studied in captive
groups of vervet monkeys, Cercopithecus aethiops sabaeus. The most frequently proposed hypotheses to explain caretaking by primate allomothers are (1) the mother benefits from the reduction in time and energy allocated to infant care, and (2) the allomother benefits by gaining maternal experience prior to the birth of her own first infant. Analysis of longitudinal data on behaviour and reproduction provided empirical support for both of these hypotheses. Mothers who used allomothers more often were able to spend more time away from their infants in the first 3 months of the infant's life, without leaving their infants alone, and were also able to shorten the interval to the birth of their next infant. Females who had more experience in caretaking and carrying infants as juveniles were more likely to rear their first live-born infant successfully. Allomothering by juvenile females was preferentially directed toward their infant siblings and toward the infants of the highest-ranking mothers.
The breeding system of many species of birds and mammals involves one or more non-parent helpers who assist in feeding and caring for the young. There is evidence for several species that alloparental assistance contributes to the survival of the young and reduces the burden of parental care on the parents (Emlen 1984; Brown 1987). Care for young by individuals other than the biological parents poses an interesting problem for evolutionary theory: for individuals to devote time and energy to the care of another's young, there should be either direct benefits to the alloparent, or indirect benefits via inclusive fitness (Hamilton 1964). The majority of alloparenting associations that have been studied are known to involve close kin, and have been consistent with the hypothesis that the alloparents are acting to increase their inclusive fitness, within systems that limit opportunities for becoming established as an independent breeder (Emlen & Wrege 1988; Mumme et al. 1989). There is also some evidence that the experience gained by alloparents can influence later success as a breeding adult (Woolfenden & Fitzpatrick 1984; Salo & French 1989). Among primates, an interest in infants by individuals other than the mother appears to be a common feature of social behaviour for the majority of species that have been studied, although the degree to which mothers permit allomothering and the relative level of interest by animals of different age and sex classes varies across species and situations 0003-3472/90/090553+10 $03.00/0
(Rowell et al. 1964; Hrdy 1976; McKenna 1979). Primate allomothering differs from cooperative breeding in birds and carnivores in several respects, however. Although there are exceptions (Pereira & Izard t989), primate allomothers typically do not provide food for the young. Many primate allomothers are immature animals who are not yet physiologically capable of breeding, and mothers frequently resist the attentions of allomothers. Three of the principle hypotheses that have been proposed to explain the occurrence of primate allomothering are: (1) immature animals benefit from allomothering by 'learning to mother', i.e. by gaining experience that will improve their ability to raise their own offspring as adults; (2) the mother benefits from allomothering by an increase in foraging efficiency and by a reduction in the time and energy required for parental care; (3) the infant benefits by receiving more protective care (Hrdy 1976). It follows that if allomothering benefits either the mother or the infant, then allomothering close kin would result in an increase in inclusive fitness for the atlomother (Johnson et al. 1980; Small & Smith 1981). It has also been suggested that in some cases primate allomothering is a competitive rather than an altruistic behaviour, and that allomothering can be more detrimental then beneficial to mothers and infants (Hrdy 1976; Silk 1980). Others have argued that primate allomothering is not adaptive, per se, but is a by-product of selection for good parenting (Quiatt 1979; Scollay & DeBold 1980).
9 1990 The Association for the Study of Animal Behaviour 553
Animal Behaviour, 40, 3
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There is some support for the hypotheses that parents, infants and allomothers all benefit from allomothering among the Callitrichidea where multiple births are common, and fathers and immature siblings typically play a major role in infant care (Locke-Hayden & Chalmers 1983; McGrew 1988; Pryce 1988). In Saguinus species, the presence of caretakers, and prior caretaking experience by the parents, have both been associated with infant survival (Epple 1978; Cleveland & Snowdon 1984; Tardifet al. 1984). Among Old World monkeys, the pattern of allomothering appears to vary considerably from species to species (Hrdy 1976; McKenna 1979). Colobine mothers voluntarily leave their infants with allomothers at an early age, while cercopithecine mothers more frequently resist the attempts of allomothers to carry their infants. Although there has been a considerable amount of speculation, there have been no published data actually measuring the costs and benefits of allomothering for the mother or for the allomother for any Old World monkey species. In the course of a longitudinal study of behaviour and social relationships in captive groups of vervet monkeys, Cercopithecus aethiops sabaeus, data have been collected on the social and reproductive consequences associated with allomothering. The analysis reported here was intended to address the hypotheses that (1) mothers benefit from allomothering by reducing their investment in their current infant and shortening the interval to the birth of their next infant, and (2) juvenile females benefit from allomothering by increasing their ability to raise their own first-born infant. If allomothering is found to be beneficial to either the allomother or to the mother, then the allocation of allomothering should be responsive to the genetic and social consequences for the parties involved. METHODS
Subjects Subjects were vervet monkeys living in four social groups at the Nonhuman Primate Research Facility, Sepulveda Veterans Administration Medical Center. The colony was established in 1975 with one group of animals captured on St Kitts, West Indies, and has subsequently been divided into two groups in 1977 and into four groups in 1986. Each of the four groups is housed in an octag-
onal outdoor enclosure, approximately 15m in diameter, with adjacent rooms for shelter from the weather. The monkeys' diet consists of commercial monkey chow, supplemented by fresh produce and by foraging in the grass. To prevent inbreeding and to approximate natural group composition, females have been kept in their natal groups, natal males have been removed at 4-5 years of age, and breeding adult males have been replaced at intervals of 3M years. When the groups were divided in 1977 and 1986, membership of the new groups was based on kinship and on patterns of affiliative behaviour prior to the split. During the period of data collection, group size ranged from 15 to 34 animals. Behavioural observations have been conducted consistently since !980 on all individuals in the four groups. Focal subjects were 27 females who have been observed from birth to the production of their first live-born infant, and 83 infants observed from birth to 6 months of age. Data are also presented for 23 infants who were born alive but died before 6 months of age.
Data Collection Behavioural interactions of all group members have been observed and recorded since 1980, using a consistent data collection system (Fairbanks & McGuire 1985; Fairbanks 1989). Data for this analysis were collected between 1980 and 1988 during focal-animal and scan samples. Each of the 27 subject females was observed for three to four 5min focal-animal samples per week and 9-12 independent scan samples per week continuously from 6 months of age to adulthood. Each of the 83 infants was observed for six to eight focal-animal samples and 18-24 scan samples per week for the first 6 months of life. During the 5-min focal-animal samples, all instances of social interaction of the focal subject with any other individual were recorded. During the instantaneous scan samples, the focal subject's spatial relationships and behavioural state were recorded. The behaviour used in this analysis included caretaking from the focal-animal samples and carrying from the scan samples. Caretaking was defined as initiating any caretaking activity including touching, grooming, inspecting, holding or trying to hold an infant by a non-mother, and was recorded once per continuous bout of activity. Carrying was recorded during scan samples when a
Fairbanks: Reciprocalbenefits of allomothering non-mother was holding or carrying an infant. The scan samples were also used to record spatial proximity of infants with their mothers and with other group members, and time spent in various behavioural states, such as resting or social play. Complete records of births, deaths and matrilineal kinship are available for all individuals living in the colony from 1975 to 1989. The term sibling is used to refer to maternal siblings.
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Data Preparation Behaviour was summarized by year of life for juveniles and by month of life for infants. Month of life was calculated from birth, in 4-week blocks, up to 6 months of age. For older individuals, data were summarized according to calendar year. An individual was designated a 1-year-old in the calendar year that contained its first birthday. A juvenile female's total allomothering experience was calculated by averaging the frequency per hour of caretaking bouts she initiated and the percentage of the time she spent carrying infants at 1 and 2 years of age. High and low levels of allomothering were determined by setting a cut-off point at the mean of each variable. To determine who directed allomothering to whom, the matrix of the frequency of caretaking by initiator and recipient was constructed for each group in each year. Females were categorized as juveniles if they were 1 or 2 years old, and as adults if they were 4 years or older. Three-year-old females were considered to be juveniles if they did not give birth in that year, and adults if they did. Between 1980 and 1988, there was an average of 4-5 juvenile females and 4.2 surviving infants per group per year, for a total of 89 juvenile female years. Fifty of the juvenile females had infant siblings. Dominance rank was determined by the direction of aggressive behaviour, recorded in the focalanimal samples and in target behaviour samples collected to supplement the focal-animal records. Females can generally be ranked in a linear dominance hierarchy, with daughters usually assuming the ranks of their mothers relative to other matrilines. Adult female rank was divided into high, middle and low, and the highest-ranking mother was identified for each year, with one exception. Females in group 3 were undergoing a rank transformation during the birth season in 1987, and it was not possible to identify a consistent highest-ranking mother for that group in that year.
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Figure l. Mean (_+SE)frequency/h that infants received caretaking from allomothers (O), and mean percentage time (_+SE)that infants were carried by allomothers (A), by month of life. (Absenceof error bars indicates that the SEis less than the height of the symbol.)
RESULTS
Description of the Behaviour Allomothering in the captive colony was remarkably similar in form and style to that described by Lancaster (t971) for east African vervets in the field. As was noted in the field, young infants were the focus of a considerable amount of attention, and new mothers were often surrounded by groups of other animals trying to touch or hold the infant. In the colony, infants received the attentions of caretakers approximately t8-19 times per hour, and were carried by allomothers an average of 10% of the time, during the first 2 months of life (Fig. 1). In the first few days after birth, almost all group members approached the mother at least once to touch, sniff and inspect the new infant. Juvenile and adult females would groom the mother and the infant, and would frequently try to pry the infant from the mother's ventrum. All group members participated in infant caretaking, but juvenile females were the most active and persistent allomothers (Table I). Juvenile females constituted 26% of the group members available to the infants in this sample, but they contributed 53% of the caretaking attempts. For 87% of the infants, the most frequent allomother was a juvenile female. Mothers differed considerably in their reactions to allomothers. Some readily allowed their infants to be carried by allomothers, even as early as the first day of life, while others avoided and resisted the attentions of caretakers throughout the first few
Animal Behaviour, 40, 3
556
Table I. Caretaking received by 83 vervet monkey infants, by age and sex of allomother
Age-sex class of allomother
Frequency/h/ individual
% of group
% of bouts
Most frequent allomother for an individual (%)
Juvenile females Adult females Natal males Adult males
1.45 0.70 0.27 0.12
26 34 31 9
53 35 12 1
87 13 0 0
months. In most cases, mothers appeared to be able to control allomothers' access to their infants.
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Mothe~infant spatial relationships The amount of time that all infants spent more than 1 m away from their mothers increased steadily from month 1 to m o n t h 6, by which time infants were away approximately 70% of the time (Fig. 2a). In the first 2 months, mothers spent up to 40% of their time away from their infants, but because of the attentions of caretakers, the infants spent virtually no time alone (Fig. 2b). Mothers whose infants were carried by allomothers more than average were able to spend more time away from their infants in the infant's first 3 months, compared to mothers whose infants were carried less than average (t=3.17, df=82, P < 0 . 0 1 ; Fig. 2a). Moreover, they accomplished this without leaving their infants alone. Infants who were carried by allomothers more than the average not only spent more time away from their mothers but they also spent less time alone in the first 3 months, compared with infants who were carried less than average (t=2.54, df=82, P < 0 . 0 1 ; Fig. 2b).
Infant mortality If allomothers were incompetent in infant handling, or overtly hostile, then the rate of infant mortality would be expected to increase with the amount of time that infants were carried by allomothers. Twenty-three infants that were born between 1980 and 1988 died within their first few months, most of unknown causes. The rate of infant
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Figure 2. Mean percentage time (_+SE) that (a) infants spent more than 1 m away from their mothers (Away), and (b) infants spent more than 1 m away from any group member (Alone), by month of life for infants carried by allomothers more ( 9 or less ( 9 than average. (Absence of error bars indicates that the SE is less than the l~eight of the symbol.)
mortality in the colony was not related to the mother's dominance rank (high: 22%; middle: 23%; low: 20%), but was influenced by the age of the mother. Young mothers (aged 3-5 years) are more likely than older mothers to lose live-born infants (Fairbanks & McGuire 1984).
Fairbanks: Reciprocalbenefits of allomothering 40~
557
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Figure3. Frequency distribution of the percentage of time that infants were carried by allomothers in the first month of life, (a) for survivinginfants (N= 83) and (b) for infants who died in the first few months of life (N= 23). To determine the contribution of allomothering to infant mortality, a comparison was made of the frequency distributions for percentage time carried by allomothers in the first month of life between the 83 surviving infants, and 23 infants who died (Fig. 3). The majority of the infants who died were never carried by allomothers. The mean values of percentage time carried by allomothers and the cumulative frequency distributions did not differ significantly between the two groups (surviving: X = 10%; dead: )?= 11%; Kolmogorov-Smirnov D = 0'32, NS). While the average amount of carrying by allomothers in the first month of life was not associated with harm to the infants, the two highest values (55 and 67%) were recorded for infants that did not survive. The mothers in both of these cases were 3year-olds who were not fully grown. Pregnancy and delivery has proven to be very stressful in this age group in the colony (Fairbanks & McGuire 1984). Both of these mothers showed signs of physical distress following delivery (hair loss, low body fat) and appeared to have voluntarily abandoned their infants. The infants in the 30-45% range on both distributions were all offspring of high-ranking females who tended to allow more caretaking than middle- and tow-ranking females (see below). Behavioural observations indicated that these
females could retrieve their infants if they chose to do so.
Mother'sfuture fecundity Vervet monkeys usually breed seasonally but, when conditions are favourable, they are capable of shortening the inter-birth interval and producing an off-season infant (Fairbanks & McGuire 1984). Between 1980 and 1988, the median inter-birth interval following the birth of a surviving infant was 12.3 months and almost all mothers gave birth again in the following year (74 of 81; five females skipped I year, and two skipped 2 years). There was a significant negative correlation between the amount of time a mother's current infant was carried by allomothers and the mother's next inter-birth interval ( r , = - 0 . 3 7 , N=81, P < 0'01; Fig. 4). Mothers who allowed their infants to be carried by allomothers more often had shorter intervals to the birth of their next infant. This relationship also held when only the females who gave birth in the next year were considered (rs = - 0'43, N = 74, P < 0"01). Since the female's dominance rank was also associated with her average inter-birth interval in this colony (Fairbanks & McGuire 1984), a stepwise
Animal Behaviour, 40, 3
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Figure 4. Scatterplot of the percentage of the time infants were carried by allomothers during the first 6 months of life, by the interval to the birth of the mother's next infant.
regression analysis was performed to determine the contribution of altomothering to inter-birth interval, independent of rank. (The seven outlying values for inter-birth interval were excluded from this analysis.) The resulting regression equation included both dominance rank and the percentage of the time the current infant was carried by allomothers as significant contributors to the prediction of the interval to the next birth (step 1: variable entered=rank, multiple R=0.44, F-to-enter= 17.46; Step 2: variable entered = % carry, multiple R = 0.49, F-to-enter = 4.23). These results are consistent with the hypothesis that allomothering benefits the mother by allowing her to shorten the interval to the birth of her next infant.
Consequences for the Juvenile Female Allomothers
Rates o f behaviour and social trade-offs Every juvenile female showed some interest in infants, but there were large individual differences in the rate of caretaking and in the percentage of time that individual females spent in allomothering. The frequency per hour ofcaretaking for the 27 females computed over the 2-year juvenile period varied from 1.6 to 6.2 bouts/h (X=3"6), and the percentage time carrying infants varied from 0.1 to 3" 1% ( 2 = 1.3%). The two measures of allomothering were independent, i.e. juvenile females who
showed a high frequency of caretaking did not necessarily spend a high percentage of the time infant carrying (r = 0'05, N = 27, Ns). Individual differences in these two behaviour patterns could not be explained by the juvenile female's matrilineal dominance rank (caretaking, bouts/h: high rank = 3.4, middle rank=3.9, low rank=3-6, F=0.47, df=2,24, ~s; carrying, percentage of the time: high rank = 1.2%, middle rank = 1.2%, low rank = 1.4%, F = 0.16, d f = 2,24, NS). The time and effort that juvenile females put into allomothering was not trivial, particularly during the birth season. To determine if there was a social cost to allomothering, the rate of caretaking was compared to the rate of aggression received and to the percentage time spent in social play during the same 2-year juvenile period. Juvenile females who initiated more caretaking received significantly more aggression from other group members ( r = 0.53, N = 2 7 , P<0"01). They also spent significantly less time involved in other forms of social play ( r = - 0 . 4 1 , N = 2 7 , P<0.05). Maternal competence as an adult Twenty-seven females who were observed as allomothers at 1 and 2 years of age produced their first live-born infant. Sixteen of the mothers were 3 years old, and 11 were 4 years or older. Ten of the 27 infants died within their first 3 months, and the remaining 17 survived. Infant mortality varied from 2 to 64 days after birth (median = 7), and the causes were listed as dehydration (4), trauma (2) and unknown (4). The ability of these young mothers to keep their first live-born infant alive could be predicted by the amount of prior atlomothering experience they had had as juveniles. Females who had spent more time carrying infants as juveniles were significantly more likely to produce surviving infants as adults (Table II). The best predictor of adult breeding success was a combination of both measures of allomothering. Females who had been above the mean on both the number of caretaking bouts initiated and the percentage of the time spent carrying infants as juveniles all produced surviving infants, compared to only 44% of the females who had been below average on one or both of the measures (Table II). These results are consistent with the hypothesis that juvenile females benefit from allomothering by gaining mothering experience prior to the birth of their own first infant.
Fairbanks: Reciprocal benefits of allomothering
559
Table II. Survivalof first live-born infant by mother's allomotheringexperienceas a juvenile Prior allomothering experience
Number survived
Number died
% Surviving
12 5
3 7
80% 42%
<0.05
9 8
4 6
69% 57%
Ns
9 8
0 10
100% 44%
< 0.01
% Time carry High Low Frequency/h caretake High Low Combined carry and caretake Both high Other
P*
*Fisher's exact test (one-tailed).
Table IlL Observed and expected number of juvenile females selecting particular infants as most frequent object of caretaking, by kinship and by the dominance rank of the infant's mother
Kinship Sibling Non-sibling Mother's rank Highest-ranking mother Other mother
Observed
Expected
28 22
11 39
52"6
<0'01
57 30
21 66
123'4
<0"01
Allocation of Allomothering Juvenile females initiated caretaking at the same rate, whether or not they had an infant sibling (females with sibling: 3-5 bouts/h; without sibling: 3.6 bouts/h; t = -0.74, Ns), but when they did have an infant sibling, they selected their sibling for caretaking more often than they selected non-kin infants. Infants received significantly more caretaking from their juvenile sisters (2-2 bouts/h) than from individual non-kinjuvenilefemales (1 '6 bouts/ h; matched t = -6.00, P < 0.01). Fifty-six per cent of the 50 juvenile females with an infant sibling directed more caretaking to their sibling than to any other infant (expected = 22%; Table III). In addition to the bias toward close kin, there was also a preference for allomothering the infants of high-ranking females. Infants of high-ranking mothers received significantlymore caretaking from juvenile females than did infants of middle- and
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low-ranking mothers (high-ranking: 1.90 bouts/h; middle- and low-ranking: 1"21 bouts/h; t = 5.05, dr= 80, P < 0"01). Sixty-six per cent of the juvenile females in the sample directed more allomothering to the infant of the highest-ranking mother available than to any other infant (expected=24%; Table III). The relative attractiveness of infant siblings and infants of high-ranking females were additive and approximately equal. When faced with the choice of directing the most caretaking to an infant sibling or the infant of the highest-ranking mother, 41% (14 of 34) of the juvenile females chose their lowerranking sibling, 44% (15 of 34) chose the unrelated infant of the highest-ranking mother, one female had a tie between an infant sibling and the infant of the highest-ranking mother, and only 12% (4 of 34, expected = 63 %) directed the most caretaking to an infant who was neither a sibling nor the infant of the highest-ranking mother. When an infant sibling
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Animal Behaviour, 40, 3
was also the infant of the highest-ranking mother, 81% (13/16) of the juvenile females directed more caretaking to their sibling than to any other infant.
DISCUSSION Benefits to the Mother
The results of this analysis demonstrate that, in the context of the captive colony, there were benefits to the mother associated with using allomothers. Mothers who used allomothers more often to carry their infants were able to shorten the interval to the birth of their next infant. Whether allomothering is beneficial to the mother should, of course, depend on the balance between the benefits in increased fecundity and the costs in infant mortality. This balance would be expected to shift both within and across species according to the attributes of the mother, the pool of allomothers, the demands of the foraging environment, and the nature of the social system (McKenna 1979; Silk 1980; Lee 1989). In this study, for example, individual differences in the use of allomothers were associated with the mother's rank, with high-ranking mothers using caretakers more often than low- ranking mothers, a pattern that has also been noted for baboons, and for east African vervet monkeys (Rowell et al. 1968; Cheney 1978; Lee 1989). This rank difference is predictable if we assume that the potential benefits of allomothering would be equal for high- and low-ranking mothers, but the costs in terms of risk to the infant's safety would be greater for low- than for high-ranking mothers. If high-ranking mothers can be more assured of retrieving their infants in case of distress, they should be more likely to allow allomothers to take them, particularly juvenile allomothers. This greater willingness to use aUomothers may in fact be the basis for high-ranking females' greater reproductive success in the vervet colony (Fairbanks & McGuire 1984). In the field, it has been suggested that the mother benefits from allomothering by being free to forage without the burden of carrying her infant (Hrdy 1976; Quiatt 1979; Whitten 1982). It is unlikely that this mechanism is operating in the captive vervet colony, however, as high-quality food is readily and continuously available. An alternate explanation for the association between shortened inter-birth interval and use of allomothers might be in longer
periods of time between nursing bouts for infants who were frequently carried by caretakers compared to infants who had more constant access to their mother's breast (McNeilly et al. 1985). In a more natural setting, both of these factors might be expected to come into play, and allomothers might be expected to have an even greater effect on the mother's reproductive success than was found here. Benefits to the Juvenile AIIomothcr
in the vervet colony, females who initiated caretaking more often and had more experience carrying infants as juveniles were more successful in raising their own first live-born infant. This association could not be explained by differences in family rank or in the availability of infant siblings. Associations of alloparenting experience and later reproductive success have also been reported for tamarins (Epple 1978; Cleveland & Snowdon 1984; Tardifet al. 1984), Florida scrub jays, Aphelicoma coerulescens (Woolfenden & Fitzpatrick 1984) and Mongolian gerbils Meriones unguiculatus (Salo & French 1989), suggesting that prior parenting experience can provide direct benefits to first-time breeders in a wide variety of species. Because the vervet females played an active part in determining how much allomothering experience they were getting, in this analysis, the effects of inherent individual differences in attraction to infants could not be separated from the actual effects of practice in infant handling, in promoting successful mothering. If we assume that there are genetically based individual differences among juvenile females in their level of interest in infants, then it would follow that females who are more interested in infants would be more likely to seek and obtain experience in infant handling, and the experience they gained in mothering could serve to increase their chances of success with their own first infant (Quiatt 1979). A genetic predisposition to create an appropriate learning environment is probably a common mechanism in behavioural development (Harper 1989), and the results of this analysis suggest that this combination of predisposition and experience could be the basis of natural selection for allomothering by juvenile females. The fact that there were social risks associated with high levels of allomothering, in addition to the investment of time and energy involved in pursuing mothers and carrying infants, suggests that allomothering is not without cost to the juvenile
Fairbanks: Reciprocal benefits o f allomothering
females. Those individuals who did more allomothering paid in terms of increased social aggression, and trade-offs in time spent in other types of play activities that are generally believed to provide long-term benefits to the individuals involved (Fagen 1981; Bekoff 1988). These costs appeared to have been offset by the gain in infanthandling experience that allowed females to raise their own first live-born infant successfully.
561
ACKNOWLEDGMENTS I thank Karin Blau, Diane Crumley, Michaela Heeb, Mary Baker and Dan Diekmann for assistance in data collection and animal care, and Michael McGuire for his dedication to the maintenance of the captive colony. This research was funded by NSF grants BNS 84-02292 and 87-09765. Computing support was provided by the Office of Academic Computing, U.C.L.A.
Allocation of Allomothering Juvenile female vervets were discriminating in the infants they chose to allomother, and selected siblings and the infants of the highest-ranking mother in the group. Caretaking of infant siblings should be promoted by many mechanisms, both proximate and ultimate, and kin preference has been noted repeatedly in studies of alloparenting (Emlen 1984). Since juvenile females still spend a considerable amount of time near their mothers, they would already be in close proximity to their infant siblings (Fairbanks & McGuire t985; Holman & Goy t988). By allowing her own daughter to caretake, a mother would be reducing her investment in her current infant while at the same time promoting the future reproductive success of her immature daughter. From the point of view of the juvenile female, the benefits given to the mother would be partially retrieved in the form of inclusive fitness. The increased preference for allomothering infants of high-ranking females is more diffficult to explain. By caretaking the infants of high-ranking mothers, a juvenile female could potentially be increasing the fitness of non-kin at the expense of kin. Hypothetically, high-ranking females should have higher value as allies and associates, compared to low-ranking animals (Seyfarth 1977; Kummer 1978; Wasser 1982), but the actual benefits received by performing altruistic acts for highranking animals have often been difficult to identify (Fairbanks 1980; Silk 1982; Harcourt 1989). Although it is possible that juvenile females might benefit by gaining the favour and tolerance of highranking females in situations that could confer protection and greater access to resources (de Waal 1989), the fact that the juvenile females benefit directly by gaining experience in infant handling has probably allowed a system of mutual cooperation to develop that does not depend entirely on future reciprocity from the high-ranking mothers.
REFERENCES Bekoff, M. 1988. Motor training and physical fitness: possible short- and long-term influenceson the development of individual differences in behavior. Devl Psychobiol., 21,601-612. Brown J. L. 1987. Ecology and Evolution of Helping and Communal Breeding in Birds. Princeton, New Jersey: Princeton University Press. Cheney, D. L. 1978. Interactions of immature male and female baboons with adult females. Anim. Behav., 26, 389-408. Cleveland,J. & Snowdon, C. T. 1984. Socialdevelopment during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus). Anita. Behav., 32, 432-444. Emlen, S. T. 1984. Cooperative breeding in birds and mammals.In: Behavioural Ecology (Ed. by J. R. Krebs & N. B. Davies),pp. 305-339.Sunderland,Massachusetts: Sinauer Associates. Emlen, S. T. & Wrege, P. H. 1988. The role of kinship in helping decisions among white-fronted bee-eaters. Behav. Ecol. Sociobiol., 23, 305-315. Epple, G. 1978. Reproductive and social behavior of marmosets with special reference to captive breeding. Primates Med., 10, 5~62. Fagen, R. 1981. Animal Play Behavior. New York: Oxford UniversityPress. Fairbanks, L. A. 1980. Relationships among females in captive vervet monkeys:testing a model of rank-related attractiveness. Anim. Behav., 28, 853 859. Fairbanks, L. A. 1989. Early experience and crossgenerational continuity of mother-infant contact in vervet monkeys. Devl Psychobiol., 22, 669 681. Fairbanks, L. A. & McGuire, M. T. 1984. Determinants of fecundity and reproductive success in captive vervet monkeys. Am. J. Primatol., 7, 27-38. Fairbanks, L. A. & McGuire, M. T. 1985. Relationships of vervet mothers with sons and daughters from one through three years of age. Anim. Behav., 33, 27-38. Harcourt, A. H. 1989. Social influences on competitive ability: alliancesand their consequences.In: Comparative Socioecology (Ed. by V. Standen & R. A. Foley), pp. 223-242. Oxford: BlackwellScientificPublications. Harper, L. V. 1989. The Nurture of Human Behavior. Norwood, New Jersey: Ablex Publishing. Hamilton, W. D. 1964. The genetical evolution of social behavior. Parts I and II. J. theor. Biol., 7, 1-52.
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Holman, S. D. & Goy, R. W. 1988. Sexually dimorphic transitions revealed in the r61ationships of yearling rhesus monkeys following the birth of siblings. Int. J. Primatol., 9, 113-133. Hrdy, S. B. 1976. Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In: Advances in the Study of Behavior. Vol. 6 (Ed. by J. S. Rosenblatt, R. A. Hinde, E. Shaw, & C. Beer), pp. 101-158. New York: Academic Press. Johnson, C. J., Koerner, C., Estrin, M. & Duoos, D. 1980. Alloparental care and kinship in captive social groups of vervet monkeys (Cercopitheeus aethiops sabaeus). Primates, 21, 406-415. Kummer, H. 1978. On the value of social relationships to nonhuman primates: a heuristic scheme. Soe. Sei. Inf., 17, 687-705. Lancaster, J. 1971. Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Foliaprimatol., 15, 161-182. Lee, P. C. 1989. Family structure, communal care and female reproductive effort. In: Comparative Soeioecology (Ed. by V. Standen & R. A. Foley), pp. 323-340. Oxford: Blackwell Scientific Publications. Locke-Hayden, J. & Chalmers, N. R. 1983. The development of infant-earegiver relationships in captive common marmosets. Int. J. Primatol., 4, 63-81. McGrew, W. C. 1988. Parental division of infant caretaking varies with family composition in cotton-top tamarins. Anim. Behav., 36, 285-310. McKenna, J. J. 1979. The evolution of allomothering behavior among colobine monkeys: function and opportunism in evolution. Am. Anthropol., 81, 818-840. McNeilly, A. S., Galsier, A. & Howie, P. W. 1985. Endocrine control oflactational infertility In: Maternal Nutrition andLaetational Infertility (Ed. by J. Dobbing), pp. 1-24. New York: Raven Press. Mumme, R. L., Koenig, W. D. & Ratnieks, F. L. 1989. Helping behaviour, reproductive value, and the future component of indirect fitness. Anim. Behav., 38, 331-343. Pereira, M. E. & Izard, M. K. 1989. Lactation and care for unrelated infants in forest-living ringtailed lemurs. Am. J. Primatol., 18, 101-108. Pryce, C. R. 1988. Individual and group effects on early caregiver-infant relationships in red-bellied tamarin monkeys. Anim. Behav., 36, 1455-1464.
Quiatt, D. 1979. Aunts and mothers: adaptive implications of allomaternal behavior of nonhuman primates. Am. Anthropol., 81,310-319. RoweU, T. E., Din, N. A. & Omar, A. 1968. The social development of baboons in their first three months. J. Zool., Lond., 155, 461-483. Rowell, T. E., Hinde, R. A. & Spencer-Booth, Y. 1964. 'Aunt'-infant interaction in captive rhesus monkeys. Anim. Behav., 12, 219-226. Salo, A. L. & French, J. A. 1989. Early experience, reproductive success and development of parental behaviour in Mongolian gerbils. Anim. Behav., 38, 693-702. Scollay, P. A. & DeBold, P. 1980. Allomothering in a captive colony of hanuman langurs (Presbytis entellus). Ethol. Soeiobiol., 1, 291-299. Seyfarth, R. M. 1977. A model of social grooming among adult female monkeys. J. theor. Biol., 65, 671-698. Silk, J. B. 1980. Kidnapping and female competition among captive bonnet macaques. Primates, 21, 100-110. Silk, J. B. 1982. Altruism among female Macaca radiata: explanations and analysis of patterns of grooming and coalition formation. Behaviour, 79, 162-188. Small, M. F. & Smith, D. G. 1981. Interactions with infants by full siblings, paternal half-siblings, and nonrelatives in a captive group of rhesus macaques (Macaca mulatta) Am. J. Primatol., 1, 91-94. Tardif, S. D., Richter, C. B. & Carson, R. L. 1984. Effects of sibling rearing experience on future reproductive success in two species ofcallitrichidae. Am. J. Primatol., 6, 377-380. de Waal, F. B. M. 1989. Dominance 'style' and primate social organization. In: Comparative Socioecology (Ed. by V. Standen & R. A. Foley), pp. 243-262. Oxford: Blackwell Scientific Publications. Wasser, S. K. 1982. Reciprocity and the trade-off between associate quality and relatedness Am. Nat., 119, 720-731. Whitten, P. L. 1982. Female reproductive strategies among vervet monkeys. Ph.D. thesis, Harvard University. Woolfenden, G. E. & Fitzpatrick, J. W. 1984. The Florida Scrub Jay: Demography of a Cooperative-breeding Bird. Princeton, New Jersey: Princeton University Press.
(Received 30 October 1989; initial acceptance 28 November 1989;final acceptance 28 January 1990; MS. number." A5667)
Reciprocal benefits of allomothering for female vervet monkeys L Y N N A. F A I R B A N K S
Department of Psychiatry and Biobehavioral Sciences, University of CaliJbrnia, Los Angeles, CA 90024 U.S.A.
Abstract. Allomothering, or care of the young by individuals other than the mother, was studied in captive
groups of vervet monkeys, Cercopithecus aethiops sabaeus. The most frequently proposed hypotheses to explain caretaking by primate allomothers are (1) the mother benefits from the reduction in time and energy allocated to infant care, and (2) the allomother benefits by gaining maternal experience prior to the birth of her own first infant. Analysis of longitudinal data on behaviour and reproduction provided empirical support for both of these hypotheses. Mothers who used allomothers more often were able to spend more time away from their infants in the first 3 months of the infant's life, without leaving their infants alone, and were also able to shorten the interval to the birth of their next infant. Females who had more experience in caretaking and carrying infants as juveniles were more likely to rear their first live-born infant successfully. Allomothering by juvenile females was preferentially directed toward their infant siblings and toward the infants of the highest-ranking mothers.
The breeding system of many species of birds and mammals involves one or more non-parent helpers who assist in feeding and caring for the young. There is evidence for several species that alloparental assistance contributes to the survival of the young and reduces the burden of parental care on the parents (Emlen 1984; Brown 1987). Care for young by individuals other than the biological parents poses an interesting problem for evolutionary theory: for individuals to devote time and energy to the care of another's young, there should be either direct benefits to the alloparent, or indirect benefits via inclusive fitness (Hamilton 1964). The majority of alloparenting associations that have been studied are known to involve close kin, and have been consistent with the hypothesis that the alloparents are acting to increase their inclusive fitness, within systems that limit opportunities for becoming established as an independent breeder (Emlen & Wrege 1988; Mumme et al. 1989). There is also some evidence that the experience gained by alloparents can influence later success as a breeding adult (Woolfenden & Fitzpatrick 1984; Salo & French 1989). Among primates, an interest in infants by individuals other than the mother appears to be a common feature of social behaviour for the majority of species that have been studied, although the degree to which mothers permit allomothering and the relative level of interest by animals of different age and sex classes varies across species and situations 0003-3472/90/090553+10 $03.00/0
(Rowell et al. 1964; Hrdy 1976; McKenna 1979). Primate allomothering differs from cooperative breeding in birds and carnivores in several respects, however. Although there are exceptions (Pereira & Izard t989), primate allomothers typically do not provide food for the young. Many primate allomothers are immature animals who are not yet physiologically capable of breeding, and mothers frequently resist the attentions of allomothers. Three of the principle hypotheses that have been proposed to explain the occurrence of primate allomothering are: (1) immature animals benefit from allomothering by 'learning to mother', i.e. by gaining experience that will improve their ability to raise their own offspring as adults; (2) the mother benefits from allomothering by an increase in foraging efficiency and by a reduction in the time and energy required for parental care; (3) the infant benefits by receiving more protective care (Hrdy 1976). It follows that if allomothering benefits either the mother or the infant, then allomothering close kin would result in an increase in inclusive fitness for the atlomother (Johnson et al. 1980; Small & Smith 1981). It has also been suggested that in some cases primate allomothering is a competitive rather than an altruistic behaviour, and that allomothering can be more detrimental then beneficial to mothers and infants (Hrdy 1976; Silk 1980). Others have argued that primate allomothering is not adaptive, per se, but is a by-product of selection for good parenting (Quiatt 1979; Scollay & DeBold 1980).
9 1990 The Association for the Study of Animal Behaviour 553
Animal Behaviour, 40, 3
554
There is some support for the hypotheses that parents, infants and allomothers all benefit from allomothering among the Callitrichidea where multiple births are common, and fathers and immature siblings typically play a major role in infant care (Locke-Hayden & Chalmers 1983; McGrew 1988; Pryce 1988). In Saguinus species, the presence of caretakers, and prior caretaking experience by the parents, have both been associated with infant survival (Epple 1978; Cleveland & Snowdon 1984; Tardifet al. 1984). Among Old World monkeys, the pattern of allomothering appears to vary considerably from species to species (Hrdy 1976; McKenna 1979). Colobine mothers voluntarily leave their infants with allomothers at an early age, while cercopithecine mothers more frequently resist the attempts of allomothers to carry their infants. Although there has been a considerable amount of speculation, there have been no published data actually measuring the costs and benefits of allomothering for the mother or for the allomother for any Old World monkey species. In the course of a longitudinal study of behaviour and social relationships in captive groups of vervet monkeys, Cercopithecus aethiops sabaeus, data have been collected on the social and reproductive consequences associated with allomothering. The analysis reported here was intended to address the hypotheses that (1) mothers benefit from allomothering by reducing their investment in their current infant and shortening the interval to the birth of their next infant, and (2) juvenile females benefit from allomothering by increasing their ability to raise their own first-born infant. If allomothering is found to be beneficial to either the allomother or to the mother, then the allocation of allomothering should be responsive to the genetic and social consequences for the parties involved. METHODS
Subjects Subjects were vervet monkeys living in four social groups at the Nonhuman Primate Research Facility, Sepulveda Veterans Administration Medical Center. The colony was established in 1975 with one group of animals captured on St Kitts, West Indies, and has subsequently been divided into two groups in 1977 and into four groups in 1986. Each of the four groups is housed in an octag-
onal outdoor enclosure, approximately 15m in diameter, with adjacent rooms for shelter from the weather. The monkeys' diet consists of commercial monkey chow, supplemented by fresh produce and by foraging in the grass. To prevent inbreeding and to approximate natural group composition, females have been kept in their natal groups, natal males have been removed at 4-5 years of age, and breeding adult males have been replaced at intervals of 3M years. When the groups were divided in 1977 and 1986, membership of the new groups was based on kinship and on patterns of affiliative behaviour prior to the split. During the period of data collection, group size ranged from 15 to 34 animals. Behavioural observations have been conducted consistently since !980 on all individuals in the four groups. Focal subjects were 27 females who have been observed from birth to the production of their first live-born infant, and 83 infants observed from birth to 6 months of age. Data are also presented for 23 infants who were born alive but died before 6 months of age.
Data Collection Behavioural interactions of all group members have been observed and recorded since 1980, using a consistent data collection system (Fairbanks & McGuire 1985; Fairbanks 1989). Data for this analysis were collected between 1980 and 1988 during focal-animal and scan samples. Each of the 27 subject females was observed for three to four 5min focal-animal samples per week and 9-12 independent scan samples per week continuously from 6 months of age to adulthood. Each of the 83 infants was observed for six to eight focal-animal samples and 18-24 scan samples per week for the first 6 months of life. During the 5-min focal-animal samples, all instances of social interaction of the focal subject with any other individual were recorded. During the instantaneous scan samples, the focal subject's spatial relationships and behavioural state were recorded. The behaviour used in this analysis included caretaking from the focal-animal samples and carrying from the scan samples. Caretaking was defined as initiating any caretaking activity including touching, grooming, inspecting, holding or trying to hold an infant by a non-mother, and was recorded once per continuous bout of activity. Carrying was recorded during scan samples when a
Fairbanks: Reciprocalbenefits of allomothering non-mother was holding or carrying an infant. The scan samples were also used to record spatial proximity of infants with their mothers and with other group members, and time spent in various behavioural states, such as resting or social play. Complete records of births, deaths and matrilineal kinship are available for all individuals living in the colony from 1975 to 1989. The term sibling is used to refer to maternal siblings.
25
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Data Preparation Behaviour was summarized by year of life for juveniles and by month of life for infants. Month of life was calculated from birth, in 4-week blocks, up to 6 months of age. For older individuals, data were summarized according to calendar year. An individual was designated a 1-year-old in the calendar year that contained its first birthday. A juvenile female's total allomothering experience was calculated by averaging the frequency per hour of caretaking bouts she initiated and the percentage of the time she spent carrying infants at 1 and 2 years of age. High and low levels of allomothering were determined by setting a cut-off point at the mean of each variable. To determine who directed allomothering to whom, the matrix of the frequency of caretaking by initiator and recipient was constructed for each group in each year. Females were categorized as juveniles if they were 1 or 2 years old, and as adults if they were 4 years or older. Three-year-old females were considered to be juveniles if they did not give birth in that year, and adults if they did. Between 1980 and 1988, there was an average of 4-5 juvenile females and 4.2 surviving infants per group per year, for a total of 89 juvenile female years. Fifty of the juvenile females had infant siblings. Dominance rank was determined by the direction of aggressive behaviour, recorded in the focalanimal samples and in target behaviour samples collected to supplement the focal-animal records. Females can generally be ranked in a linear dominance hierarchy, with daughters usually assuming the ranks of their mothers relative to other matrilines. Adult female rank was divided into high, middle and low, and the highest-ranking mother was identified for each year, with one exception. Females in group 3 were undergoing a rank transformation during the birth season in 1987, and it was not possible to identify a consistent highest-ranking mother for that group in that year.
555
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0
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6
Figure l. Mean (_+SE)frequency/h that infants received caretaking from allomothers (O), and mean percentage time (_+SE)that infants were carried by allomothers (A), by month of life. (Absenceof error bars indicates that the SEis less than the height of the symbol.)
RESULTS
Description of the Behaviour Allomothering in the captive colony was remarkably similar in form and style to that described by Lancaster (t971) for east African vervets in the field. As was noted in the field, young infants were the focus of a considerable amount of attention, and new mothers were often surrounded by groups of other animals trying to touch or hold the infant. In the colony, infants received the attentions of caretakers approximately t8-19 times per hour, and were carried by allomothers an average of 10% of the time, during the first 2 months of life (Fig. 1). In the first few days after birth, almost all group members approached the mother at least once to touch, sniff and inspect the new infant. Juvenile and adult females would groom the mother and the infant, and would frequently try to pry the infant from the mother's ventrum. All group members participated in infant caretaking, but juvenile females were the most active and persistent allomothers (Table I). Juvenile females constituted 26% of the group members available to the infants in this sample, but they contributed 53% of the caretaking attempts. For 87% of the infants, the most frequent allomother was a juvenile female. Mothers differed considerably in their reactions to allomothers. Some readily allowed their infants to be carried by allomothers, even as early as the first day of life, while others avoided and resisted the attentions of caretakers throughout the first few
Animal Behaviour, 40, 3
556
Table I. Caretaking received by 83 vervet monkey infants, by age and sex of allomother
Age-sex class of allomother
Frequency/h/ individual
% of group
% of bouts
Most frequent allomother for an individual (%)
Juvenile females Adult females Natal males Adult males
1.45 0.70 0.27 0.12
26 34 31 9
53 35 12 1
87 13 0 0
months. In most cases, mothers appeared to be able to control allomothers' access to their infants.
80 (a) 70 60
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Mothe~infant spatial relationships The amount of time that all infants spent more than 1 m away from their mothers increased steadily from month 1 to m o n t h 6, by which time infants were away approximately 70% of the time (Fig. 2a). In the first 2 months, mothers spent up to 40% of their time away from their infants, but because of the attentions of caretakers, the infants spent virtually no time alone (Fig. 2b). Mothers whose infants were carried by allomothers more than average were able to spend more time away from their infants in the infant's first 3 months, compared to mothers whose infants were carried less than average (t=3.17, df=82, P < 0 . 0 1 ; Fig. 2a). Moreover, they accomplished this without leaving their infants alone. Infants who were carried by allomothers more than the average not only spent more time away from their mothers but they also spent less time alone in the first 3 months, compared with infants who were carried less than average (t=2.54, df=82, P < 0 . 0 1 ; Fig. 2b).
Infant mortality If allomothers were incompetent in infant handling, or overtly hostile, then the rate of infant mortality would be expected to increase with the amount of time that infants were carried by allomothers. Twenty-three infants that were born between 1980 and 1988 died within their first few months, most of unknown causes. The rate of infant
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Figure 2. Mean percentage time (_+SE) that (a) infants spent more than 1 m away from their mothers (Away), and (b) infants spent more than 1 m away from any group member (Alone), by month of life for infants carried by allomothers more ( 9 or less ( 9 than average. (Absence of error bars indicates that the SE is less than the l~eight of the symbol.)
mortality in the colony was not related to the mother's dominance rank (high: 22%; middle: 23%; low: 20%), but was influenced by the age of the mother. Young mothers (aged 3-5 years) are more likely than older mothers to lose live-born infants (Fairbanks & McGuire 1984).
Fairbanks: Reciprocalbenefits of allomothering 40~
557
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Figure3. Frequency distribution of the percentage of time that infants were carried by allomothers in the first month of life, (a) for survivinginfants (N= 83) and (b) for infants who died in the first few months of life (N= 23). To determine the contribution of allomothering to infant mortality, a comparison was made of the frequency distributions for percentage time carried by allomothers in the first month of life between the 83 surviving infants, and 23 infants who died (Fig. 3). The majority of the infants who died were never carried by allomothers. The mean values of percentage time carried by allomothers and the cumulative frequency distributions did not differ significantly between the two groups (surviving: X = 10%; dead: )?= 11%; Kolmogorov-Smirnov D = 0'32, NS). While the average amount of carrying by allomothers in the first month of life was not associated with harm to the infants, the two highest values (55 and 67%) were recorded for infants that did not survive. The mothers in both of these cases were 3year-olds who were not fully grown. Pregnancy and delivery has proven to be very stressful in this age group in the colony (Fairbanks & McGuire 1984). Both of these mothers showed signs of physical distress following delivery (hair loss, low body fat) and appeared to have voluntarily abandoned their infants. The infants in the 30-45% range on both distributions were all offspring of high-ranking females who tended to allow more caretaking than middle- and tow-ranking females (see below). Behavioural observations indicated that these
females could retrieve their infants if they chose to do so.
Mother'sfuture fecundity Vervet monkeys usually breed seasonally but, when conditions are favourable, they are capable of shortening the inter-birth interval and producing an off-season infant (Fairbanks & McGuire 1984). Between 1980 and 1988, the median inter-birth interval following the birth of a surviving infant was 12.3 months and almost all mothers gave birth again in the following year (74 of 81; five females skipped I year, and two skipped 2 years). There was a significant negative correlation between the amount of time a mother's current infant was carried by allomothers and the mother's next inter-birth interval ( r , = - 0 . 3 7 , N=81, P < 0'01; Fig. 4). Mothers who allowed their infants to be carried by allomothers more often had shorter intervals to the birth of their next infant. This relationship also held when only the females who gave birth in the next year were considered (rs = - 0'43, N = 74, P < 0"01). Since the female's dominance rank was also associated with her average inter-birth interval in this colony (Fairbanks & McGuire 1984), a stepwise
Animal Behaviour, 40, 3
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Figure 4. Scatterplot of the percentage of the time infants were carried by allomothers during the first 6 months of life, by the interval to the birth of the mother's next infant.
regression analysis was performed to determine the contribution of altomothering to inter-birth interval, independent of rank. (The seven outlying values for inter-birth interval were excluded from this analysis.) The resulting regression equation included both dominance rank and the percentage of the time the current infant was carried by allomothers as significant contributors to the prediction of the interval to the next birth (step 1: variable entered=rank, multiple R=0.44, F-to-enter= 17.46; Step 2: variable entered = % carry, multiple R = 0.49, F-to-enter = 4.23). These results are consistent with the hypothesis that allomothering benefits the mother by allowing her to shorten the interval to the birth of her next infant.
Consequences for the Juvenile Female Allomothers
Rates o f behaviour and social trade-offs Every juvenile female showed some interest in infants, but there were large individual differences in the rate of caretaking and in the percentage of time that individual females spent in allomothering. The frequency per hour ofcaretaking for the 27 females computed over the 2-year juvenile period varied from 1.6 to 6.2 bouts/h (X=3"6), and the percentage time carrying infants varied from 0.1 to 3" 1% ( 2 = 1.3%). The two measures of allomothering were independent, i.e. juvenile females who
showed a high frequency of caretaking did not necessarily spend a high percentage of the time infant carrying (r = 0'05, N = 27, Ns). Individual differences in these two behaviour patterns could not be explained by the juvenile female's matrilineal dominance rank (caretaking, bouts/h: high rank = 3.4, middle rank=3.9, low rank=3-6, F=0.47, df=2,24, ~s; carrying, percentage of the time: high rank = 1.2%, middle rank = 1.2%, low rank = 1.4%, F = 0.16, d f = 2,24, NS). The time and effort that juvenile females put into allomothering was not trivial, particularly during the birth season. To determine if there was a social cost to allomothering, the rate of caretaking was compared to the rate of aggression received and to the percentage time spent in social play during the same 2-year juvenile period. Juvenile females who initiated more caretaking received significantly more aggression from other group members ( r = 0.53, N = 2 7 , P<0"01). They also spent significantly less time involved in other forms of social play ( r = - 0 . 4 1 , N = 2 7 , P<0.05). Maternal competence as an adult Twenty-seven females who were observed as allomothers at 1 and 2 years of age produced their first live-born infant. Sixteen of the mothers were 3 years old, and 11 were 4 years or older. Ten of the 27 infants died within their first 3 months, and the remaining 17 survived. Infant mortality varied from 2 to 64 days after birth (median = 7), and the causes were listed as dehydration (4), trauma (2) and unknown (4). The ability of these young mothers to keep their first live-born infant alive could be predicted by the amount of prior atlomothering experience they had had as juveniles. Females who had spent more time carrying infants as juveniles were significantly more likely to produce surviving infants as adults (Table II). The best predictor of adult breeding success was a combination of both measures of allomothering. Females who had been above the mean on both the number of caretaking bouts initiated and the percentage of the time spent carrying infants as juveniles all produced surviving infants, compared to only 44% of the females who had been below average on one or both of the measures (Table II). These results are consistent with the hypothesis that juvenile females benefit from allomothering by gaining mothering experience prior to the birth of their own first infant.
Fairbanks: Reciprocal benefits of allomothering
559
Table II. Survivalof first live-born infant by mother's allomotheringexperienceas a juvenile Prior allomothering experience
Number survived
Number died
% Surviving
12 5
3 7
80% 42%
<0.05
9 8
4 6
69% 57%
Ns
9 8
0 10
100% 44%
< 0.01
% Time carry High Low Frequency/h caretake High Low Combined carry and caretake Both high Other
P*
*Fisher's exact test (one-tailed).
Table IlL Observed and expected number of juvenile females selecting particular infants as most frequent object of caretaking, by kinship and by the dominance rank of the infant's mother
Kinship Sibling Non-sibling Mother's rank Highest-ranking mother Other mother
Observed
Expected
28 22
11 39
52"6
<0'01
57 30
21 66
123'4
<0"01
Allocation of Allomothering Juvenile females initiated caretaking at the same rate, whether or not they had an infant sibling (females with sibling: 3-5 bouts/h; without sibling: 3.6 bouts/h; t = -0.74, Ns), but when they did have an infant sibling, they selected their sibling for caretaking more often than they selected non-kin infants. Infants received significantly more caretaking from their juvenile sisters (2-2 bouts/h) than from individual non-kinjuvenilefemales (1 '6 bouts/ h; matched t = -6.00, P < 0.01). Fifty-six per cent of the 50 juvenile females with an infant sibling directed more caretaking to their sibling than to any other infant (expected = 22%; Table III). In addition to the bias toward close kin, there was also a preference for allomothering the infants of high-ranking females. Infants of high-ranking mothers received significantlymore caretaking from juvenile females than did infants of middle- and
Z2
P
low-ranking mothers (high-ranking: 1.90 bouts/h; middle- and low-ranking: 1"21 bouts/h; t = 5.05, dr= 80, P < 0"01). Sixty-six per cent of the juvenile females in the sample directed more allomothering to the infant of the highest-ranking mother available than to any other infant (expected=24%; Table III). The relative attractiveness of infant siblings and infants of high-ranking females were additive and approximately equal. When faced with the choice of directing the most caretaking to an infant sibling or the infant of the highest-ranking mother, 41% (14 of 34) of the juvenile females chose their lowerranking sibling, 44% (15 of 34) chose the unrelated infant of the highest-ranking mother, one female had a tie between an infant sibling and the infant of the highest-ranking mother, and only 12% (4 of 34, expected = 63 %) directed the most caretaking to an infant who was neither a sibling nor the infant of the highest-ranking mother. When an infant sibling
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was also the infant of the highest-ranking mother, 81% (13/16) of the juvenile females directed more caretaking to their sibling than to any other infant.
DISCUSSION Benefits to the Mother
The results of this analysis demonstrate that, in the context of the captive colony, there were benefits to the mother associated with using allomothers. Mothers who used allomothers more often to carry their infants were able to shorten the interval to the birth of their next infant. Whether allomothering is beneficial to the mother should, of course, depend on the balance between the benefits in increased fecundity and the costs in infant mortality. This balance would be expected to shift both within and across species according to the attributes of the mother, the pool of allomothers, the demands of the foraging environment, and the nature of the social system (McKenna 1979; Silk 1980; Lee 1989). In this study, for example, individual differences in the use of allomothers were associated with the mother's rank, with high-ranking mothers using caretakers more often than low- ranking mothers, a pattern that has also been noted for baboons, and for east African vervet monkeys (Rowell et al. 1968; Cheney 1978; Lee 1989). This rank difference is predictable if we assume that the potential benefits of allomothering would be equal for high- and low-ranking mothers, but the costs in terms of risk to the infant's safety would be greater for low- than for high-ranking mothers. If high-ranking mothers can be more assured of retrieving their infants in case of distress, they should be more likely to allow allomothers to take them, particularly juvenile allomothers. This greater willingness to use aUomothers may in fact be the basis for high-ranking females' greater reproductive success in the vervet colony (Fairbanks & McGuire 1984). In the field, it has been suggested that the mother benefits from allomothering by being free to forage without the burden of carrying her infant (Hrdy 1976; Quiatt 1979; Whitten 1982). It is unlikely that this mechanism is operating in the captive vervet colony, however, as high-quality food is readily and continuously available. An alternate explanation for the association between shortened inter-birth interval and use of allomothers might be in longer
periods of time between nursing bouts for infants who were frequently carried by caretakers compared to infants who had more constant access to their mother's breast (McNeilly et al. 1985). In a more natural setting, both of these factors might be expected to come into play, and allomothers might be expected to have an even greater effect on the mother's reproductive success than was found here. Benefits to the Juvenile AIIomothcr
in the vervet colony, females who initiated caretaking more often and had more experience carrying infants as juveniles were more successful in raising their own first live-born infant. This association could not be explained by differences in family rank or in the availability of infant siblings. Associations of alloparenting experience and later reproductive success have also been reported for tamarins (Epple 1978; Cleveland & Snowdon 1984; Tardifet al. 1984), Florida scrub jays, Aphelicoma coerulescens (Woolfenden & Fitzpatrick 1984) and Mongolian gerbils Meriones unguiculatus (Salo & French 1989), suggesting that prior parenting experience can provide direct benefits to first-time breeders in a wide variety of species. Because the vervet females played an active part in determining how much allomothering experience they were getting, in this analysis, the effects of inherent individual differences in attraction to infants could not be separated from the actual effects of practice in infant handling, in promoting successful mothering. If we assume that there are genetically based individual differences among juvenile females in their level of interest in infants, then it would follow that females who are more interested in infants would be more likely to seek and obtain experience in infant handling, and the experience they gained in mothering could serve to increase their chances of success with their own first infant (Quiatt 1979). A genetic predisposition to create an appropriate learning environment is probably a common mechanism in behavioural development (Harper 1989), and the results of this analysis suggest that this combination of predisposition and experience could be the basis of natural selection for allomothering by juvenile females. The fact that there were social risks associated with high levels of allomothering, in addition to the investment of time and energy involved in pursuing mothers and carrying infants, suggests that allomothering is not without cost to the juvenile
Fairbanks: Reciprocal benefits o f allomothering
females. Those individuals who did more allomothering paid in terms of increased social aggression, and trade-offs in time spent in other types of play activities that are generally believed to provide long-term benefits to the individuals involved (Fagen 1981; Bekoff 1988). These costs appeared to have been offset by the gain in infanthandling experience that allowed females to raise their own first live-born infant successfully.
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ACKNOWLEDGMENTS I thank Karin Blau, Diane Crumley, Michaela Heeb, Mary Baker and Dan Diekmann for assistance in data collection and animal care, and Michael McGuire for his dedication to the maintenance of the captive colony. This research was funded by NSF grants BNS 84-02292 and 87-09765. Computing support was provided by the Office of Academic Computing, U.C.L.A.
Allocation of Allomothering Juvenile female vervets were discriminating in the infants they chose to allomother, and selected siblings and the infants of the highest-ranking mother in the group. Caretaking of infant siblings should be promoted by many mechanisms, both proximate and ultimate, and kin preference has been noted repeatedly in studies of alloparenting (Emlen 1984). Since juvenile females still spend a considerable amount of time near their mothers, they would already be in close proximity to their infant siblings (Fairbanks & McGuire t985; Holman & Goy t988). By allowing her own daughter to caretake, a mother would be reducing her investment in her current infant while at the same time promoting the future reproductive success of her immature daughter. From the point of view of the juvenile female, the benefits given to the mother would be partially retrieved in the form of inclusive fitness. The increased preference for allomothering infants of high-ranking females is more diffficult to explain. By caretaking the infants of high-ranking mothers, a juvenile female could potentially be increasing the fitness of non-kin at the expense of kin. Hypothetically, high-ranking females should have higher value as allies and associates, compared to low-ranking animals (Seyfarth 1977; Kummer 1978; Wasser 1982), but the actual benefits received by performing altruistic acts for highranking animals have often been difficult to identify (Fairbanks 1980; Silk 1982; Harcourt 1989). Although it is possible that juvenile females might benefit by gaining the favour and tolerance of highranking females in situations that could confer protection and greater access to resources (de Waal 1989), the fact that the juvenile females benefit directly by gaining experience in infant handling has probably allowed a system of mutual cooperation to develop that does not depend entirely on future reciprocity from the high-ranking mothers.
REFERENCES Bekoff, M. 1988. Motor training and physical fitness: possible short- and long-term influenceson the development of individual differences in behavior. Devl Psychobiol., 21,601-612. Brown J. L. 1987. Ecology and Evolution of Helping and Communal Breeding in Birds. Princeton, New Jersey: Princeton University Press. Cheney, D. L. 1978. Interactions of immature male and female baboons with adult females. Anim. Behav., 26, 389-408. Cleveland,J. & Snowdon, C. T. 1984. Socialdevelopment during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus). Anita. Behav., 32, 432-444. Emlen, S. T. 1984. Cooperative breeding in birds and mammals.In: Behavioural Ecology (Ed. by J. R. Krebs & N. B. Davies),pp. 305-339.Sunderland,Massachusetts: Sinauer Associates. Emlen, S. T. & Wrege, P. H. 1988. The role of kinship in helping decisions among white-fronted bee-eaters. Behav. Ecol. Sociobiol., 23, 305-315. Epple, G. 1978. Reproductive and social behavior of marmosets with special reference to captive breeding. Primates Med., 10, 5~62. Fagen, R. 1981. Animal Play Behavior. New York: Oxford UniversityPress. Fairbanks, L. A. 1980. Relationships among females in captive vervet monkeys:testing a model of rank-related attractiveness. Anim. Behav., 28, 853 859. Fairbanks, L. A. 1989. Early experience and crossgenerational continuity of mother-infant contact in vervet monkeys. Devl Psychobiol., 22, 669 681. Fairbanks, L. A. & McGuire, M. T. 1984. Determinants of fecundity and reproductive success in captive vervet monkeys. Am. J. Primatol., 7, 27-38. Fairbanks, L. A. & McGuire, M. T. 1985. Relationships of vervet mothers with sons and daughters from one through three years of age. Anim. Behav., 33, 27-38. Harcourt, A. H. 1989. Social influences on competitive ability: alliancesand their consequences.In: Comparative Socioecology (Ed. by V. Standen & R. A. Foley), pp. 223-242. Oxford: BlackwellScientificPublications. Harper, L. V. 1989. The Nurture of Human Behavior. Norwood, New Jersey: Ablex Publishing. Hamilton, W. D. 1964. The genetical evolution of social behavior. Parts I and II. J. theor. Biol., 7, 1-52.
562
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Holman, S. D. & Goy, R. W. 1988. Sexually dimorphic transitions revealed in the r61ationships of yearling rhesus monkeys following the birth of siblings. Int. J. Primatol., 9, 113-133. Hrdy, S. B. 1976. Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In: Advances in the Study of Behavior. Vol. 6 (Ed. by J. S. Rosenblatt, R. A. Hinde, E. Shaw, & C. Beer), pp. 101-158. New York: Academic Press. Johnson, C. J., Koerner, C., Estrin, M. & Duoos, D. 1980. Alloparental care and kinship in captive social groups of vervet monkeys (Cercopitheeus aethiops sabaeus). Primates, 21, 406-415. Kummer, H. 1978. On the value of social relationships to nonhuman primates: a heuristic scheme. Soe. Sei. Inf., 17, 687-705. Lancaster, J. 1971. Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Foliaprimatol., 15, 161-182. Lee, P. C. 1989. Family structure, communal care and female reproductive effort. In: Comparative Soeioecology (Ed. by V. Standen & R. A. Foley), pp. 323-340. Oxford: Blackwell Scientific Publications. Locke-Hayden, J. & Chalmers, N. R. 1983. The development of infant-earegiver relationships in captive common marmosets. Int. J. Primatol., 4, 63-81. McGrew, W. C. 1988. Parental division of infant caretaking varies with family composition in cotton-top tamarins. Anim. Behav., 36, 285-310. McKenna, J. J. 1979. The evolution of allomothering behavior among colobine monkeys: function and opportunism in evolution. Am. Anthropol., 81, 818-840. McNeilly, A. S., Galsier, A. & Howie, P. W. 1985. Endocrine control oflactational infertility In: Maternal Nutrition andLaetational Infertility (Ed. by J. Dobbing), pp. 1-24. New York: Raven Press. Mumme, R. L., Koenig, W. D. & Ratnieks, F. L. 1989. Helping behaviour, reproductive value, and the future component of indirect fitness. Anim. Behav., 38, 331-343. Pereira, M. E. & Izard, M. K. 1989. Lactation and care for unrelated infants in forest-living ringtailed lemurs. Am. J. Primatol., 18, 101-108. Pryce, C. R. 1988. Individual and group effects on early caregiver-infant relationships in red-bellied tamarin monkeys. Anim. Behav., 36, 1455-1464.
Quiatt, D. 1979. Aunts and mothers: adaptive implications of allomaternal behavior of nonhuman primates. Am. Anthropol., 81,310-319. RoweU, T. E., Din, N. A. & Omar, A. 1968. The social development of baboons in their first three months. J. Zool., Lond., 155, 461-483. Rowell, T. E., Hinde, R. A. & Spencer-Booth, Y. 1964. 'Aunt'-infant interaction in captive rhesus monkeys. Anim. Behav., 12, 219-226. Salo, A. L. & French, J. A. 1989. Early experience, reproductive success and development of parental behaviour in Mongolian gerbils. Anim. Behav., 38, 693-702. Scollay, P. A. & DeBold, P. 1980. Allomothering in a captive colony of hanuman langurs (Presbytis entellus). Ethol. Soeiobiol., 1, 291-299. Seyfarth, R. M. 1977. A model of social grooming among adult female monkeys. J. theor. Biol., 65, 671-698. Silk, J. B. 1980. Kidnapping and female competition among captive bonnet macaques. Primates, 21, 100-110. Silk, J. B. 1982. Altruism among female Macaca radiata: explanations and analysis of patterns of grooming and coalition formation. Behaviour, 79, 162-188. Small, M. F. & Smith, D. G. 1981. Interactions with infants by full siblings, paternal half-siblings, and nonrelatives in a captive group of rhesus macaques (Macaca mulatta) Am. J. Primatol., 1, 91-94. Tardif, S. D., Richter, C. B. & Carson, R. L. 1984. Effects of sibling rearing experience on future reproductive success in two species ofcallitrichidae. Am. J. Primatol., 6, 377-380. de Waal, F. B. M. 1989. Dominance 'style' and primate social organization. In: Comparative Socioecology (Ed. by V. Standen & R. A. Foley), pp. 243-262. Oxford: Blackwell Scientific Publications. Wasser, S. K. 1982. Reciprocity and the trade-off between associate quality and relatedness Am. Nat., 119, 720-731. Whitten, P. L. 1982. Female reproductive strategies among vervet monkeys. Ph.D. thesis, Harvard University. Woolfenden, G. E. & Fitzpatrick, J. W. 1984. The Florida Scrub Jay: Demography of a Cooperative-breeding Bird. Princeton, New Jersey: Princeton University Press.
(Received 30 October 1989; initial acceptance 28 November 1989;final acceptance 28 January 1990; MS. number." A5667)