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Behavioral and mammary responses of adult female rhesus to strange infants
HORMONES
AND
Behavioral
BEHAVIOR
14, 348-357 (1980)
and Mammary Responses of Adult Female Rhesus to Strange Infants S.D.
HOLMAN AND R. W.Gou
Wisconsin Regional Primate Research Center, University of Wisconsin, 1223 Capitol Court, Madison, Wisconsin 53706 Approximately 90% of gonadally intact, ovariectomized, or postmenopausal feral-born multiparous rhesus macaques immediately behaved maternally and displayed strong attachment to unfamiliar neonatal rhesus infants offered to them, even though the females had not lived with infants for at least 12 months. Females showing such behavior and attachment also showed fluid secretion from their nipples even, in some cases, without oral stimulation of the nipples by the infant. Adult laboratory-reared nulliparous females did not adopt infants, although identically reared primiparous females adequately cared for their own first infants.
In natural troops or groups living in laboratories, female primates occasionally permanently adopt solitary young infants (Hinde, 1965; Marsden and Vessey, 1968; van Wulfften Palthe, and van Hoof, 1975; Welker, 1977) or kidnap infants not allowing their natural mothers to retrieve them (Bullerman, 1950; Rosenblum, 1971; Quiatt, 1977). Although adoptions may not always save the solitary infant and kidnappings work to the infant’s disadvantage, the occurrence of these activities reflects the value of the infant as an object for possession by young and adult females (Jay, 1962; Sugiyama, 1965; Lancaster, 1971; Rosenblum, 1972). During the early birth season, young nulliparous female rhesus macaques living in social groups are often observed touching, grooming (Rowell, Hinde, and Spencer-Booth, 1964), holding ventroventrally, and carrying infants (Holman, Yoshihara, and Goy in preparation). In a more experimental situation, Rosenblum (1972) has found that full-term pregnant squirrel monkeys, as well as immature females, retrieve “abandoned” infants more frequently than do other age/sex classes. Multiparous rhesus monkeys, whose infants had been removed within a few hours after birth, readily accepted and cared for another female’s newborn when it was presented to them within a few days of their own parturition (Deets and Harlow, 1974). Unexamined in that study, however, is the question of whether recent parturition and the presence of ovarian hormones are crucial for the facilitation of maternal behavior. 348 0018-506X/80/040348-10$01.00/0 Copyright @ 1980 by Academic Press, Inc. All rights of reproduction in any form reserved.
MATERNAL
RESPONSES
TO RHESUS
INFANTS
349
This report provides a description of the phenomenon of adoption experimentally evoked in adult female rhesus monkeys (Mucaca mulatta) housed alone for at least 12 months, and examines the influence of parity, rearing, and ovarian hormones on this behavioral response. METHODS Subjects Experimental females. Twenty-five mature female rhesus monkeys were classified into one nulliparous and three multiparous groups. The feral-born multiparous monkeys consisted of females (INTACT; mean age, 15.6 years) that had regular menstrual cycles (N = 7), females )OVX; mean age, 18.9 years) whose ovaries had been removed at least 19 months previously (N = 6), and aged females (MENOP; mean age estimated to be greater than 25 years) that had ceased having regular menstrual cycles at least 32 months previously (N = 6). Females in this last category were judged to be postmenopausal as in all cases a IZmonth period had elpased without menstrual bleeding. Hormonally, these females were similar to ovariectomized females with high gonadotropins and low estradiol and progesterone levels (Robinson and Bridson, personal communication). The nulliparous group, laboratory born and reared (NULLIP; mean age, 7.1 years) had regular menstrual cycles. All 25 females had been housed alone for at least 14 months, with a mean value of 67.4 months. It is important to point out that the nulliparous females used in this study were not reared in social isolation. For the first year of life they lived continuously in small groups consisting of their own mothers and four or five other mothers and infants of both sexes. They were weaned at 1 year of age and from then on lived continuously with the age-mates they had lived with during the first year except for short periods when they were separated for purposes of behavioral study. Thus these females were not socially deprived except in the sense that the composition of their social group was not as complex as that usually prevailing for feral animals. A second group of females (PRIMIP; mean age, 4.9 years, N = 6) took part in this study. These were females that had been born and reared in the laboratory and had recently given birth to their first infant. This group was not manipulated in any way. The females were housed in single cages under a 12-12 light cycle. Purina Monkey Chow was made available each morning with fresh fruit supplementing this diet occasionally. Water was continuously available. Experimental infants. Forty-three infants, aged between 2 and 12 days, were used as stimulus animals in the behavioral tests. As the infant physically matures and its movements become coordinated, its behavioral role in the regulation of the infant/experimental female interaction becomes more important. Although in this study the infants used were as young and immature as possible, some experimental females had to be
350
HOLMANANDGOY
quite active in keeping some of the struggling position.
infants in a ventroventral
PROCEDURE
Each experimental female (from groups INTACT, OVX, MENOP, AND NULLIP) was housed in the behavioral testing cage (0.75 x 1.5 x I. 15 m high) approximately 24 hr before the adoption tests began. The female was removed from the cage, a strange infant placed in the cage, and the female allowed to return. The duration of the test was 1 hr, after which the infant was removed. Such tests were given to each female on 5 separate days. Tests were occasionally extended, particularly in those cases where the female’s maternal responses were minimal (two multiparous females and three nulliparous females). Scheduling of tests depended on the availability of infants, but, on average, all five tests for a given female were completed within 7 days. The experimental females were presented with one male and one female infant; some females were presented with a different infant in each test. Before, intermittently, during, and after the behavioral testing series each female was examined for secretions from her nipples. This was carried out by manually palpating the area around the nipple and then gently squeezing the nipple. This simple procedure proved adequate for exuding any fluid present in the mammary ducts. Since in most cases the volume of nipple fluid produced was too small to analyze its constituents biochemically, a color coding system, which has been used to grade the quality of rhesus’ milk, was used. Immediately following weaning, milk in rhesus mothers runs through a number of consistency stages starting as a thick white liquid (fluid consistency score = 3) and ending 3 or 4 days later as a thin watery liquid (fluid consistency score = 1). Milk production ceases soon after this final stage (personal observation). The PRIMIP females were observed in their home cages for 1 hr with their own infants beginning a few days after they had given birth. Five such observations were carried out on 5 subsequent days. Behavior
Patterns
and Their Measurement
A check sheet, divided into 15-set intervals, was used to record behavior during the tests (groups, INTACT, OVX, MENOP, and NULLIP) as well as during the hour-long observations of the primiparous females. Each behavior was recorded only once during each interval regardless of the frequency with which it was displayed during that interval. The behavioral criteria (described below) used to define maternally related behavior were established from pilot studies and from published material on rhesus maternal behavior (Harlow, Harlow, and Hansen, 1963; Hansen, 1966; Seay, 1966). Approach. Animal (infant or female) approaches partner to within 60 cm.
MATERNAL
RESPONSES
351
TO RHESUS INFANTS
Leave. Animal moves at least 60 cm away from partner. Animal interdistance (AID). The frequency of 15set intervals or parts of 1%set intervals that the animal was under (AID < 60) or over (AID > 60) 60 cm. Lipsmack. Adult female moves lips rapidly in a kissing fashion with smacking sounds. The female’s head is usually turned toward infant. This behavior pattern is thought to be a nonhostile, friendly gesture although it is often seen in what seem to be contexts of mild apprehension. Groom. Female grooms infant’s pelage; the fur on the infant’s back or around its genital area is usually groomed. The female often lipsmacks during initiation of grooming. Touch. The female physically handles and manipulates the infant, for example, during visual examination and inspection of the infant. Restrain. Whether or not the female had to be physically restrained while the infant was forcibly removed at the end of the test was recorded. For some of the behavioral patterns latency was estimated to the nearest 15set interval from beginning of the test to the occurrence of the particular response. Statistical analyses were performed on the medians of the median frequencies for behavioLs. RESULTS
Behavioral Responses The major factor affecting the nature of the responses shown by adult females toward the infants was prior parity (Table 1). Seventeen of the nineteen multiparous females tested retrieved and held the infant in a ventroventral position, and they did so on all five tests. Nulliparous females never retrieved or held the infant ventroventrally. Similarly, the two multiparous females that failed to pick up and hold the infants offered behaved consistently on all five tests. As shown in Table 1 all multiparous females that retrieved and held the infant had to be physically restrained at the end of the test and the infant was forcibly removed. This procedure was unnecessary with any of the nulliparous females. No multiparous female that held an infant ever abandoned that infant when the test ended and the female reentered the transport box. When she did so, she carried Responses of Multiparous
Response % Retrieving % Holding ventroventral % Restrained
TABLE 1 and Mulliparous Adult Rhesus Females to Unfamiliar Neonates Nulliparous (N = 6) 0 0 0
Multiparous (all types combined N = 19) 89.5 89.5 89.5
352
HOLMAN
AND
GOY
the infant with her. In short, for these three types of behavioral events (retrieving, holding, and the need for physical restraint to affect separation) the females tested responded in an all-or-none fashion and their pattern of response was consistent from test to test. The failure to respond positively toward an infant was a conspicuously consistent trait of some females. The one nulliparous and two multiparous females that failed to retrieve or hold infants in the standardized test were allowed to live continuously for 10 days with a bottle-fed infant. Throughout this period, they never held the infant during the hour-long daily observation. In addition, two nulliparous females were tested daily in 2-hr sessions for 10 days. Neither ever retrieved or held the infants. Neither in the special circumstances described in the preceding paragraph nor in the standardized tests were hostile responses toward the infants shown by females failing to retrieve and hold. Characteristically, such females were indifferent to the infants offered. Occasionally during the standardized tests, however, some affiliative responses to the infants were shown by nulliparous females. For example, nulliparous females sat near the infant (AID < 60 cm) during 69 of the possible 240 15-set intervals on average (range of individual medians over the five tests was 24 to 150 15-set intervals). But multiparous females were within 60 cm of the infant during 240 15-set intervals on average (range 128-240, Mann-Whitney U = 112.0, P < 0.002). Grooming the infant was observed during a maximum of five 15-set intervals (overall median = 0) for nulliparous compared with a median of 18 intervals (range 0 to 80) for multiparous females (U = 103.5, P < 0.002). Touching the infant, while not frequent among nulliparous females (median 0, range 0 to 27), occurred during nineteen 15-set intervals on average for multiparous females (range 0 to 90, U = 99.0, P < 0.01). Lipsmacking was the only response displayed nearly equally often by nulliparous (median = 7, range I to 28) and multiparous (median = 10, range 5 to 92) females. The variations in endocrine status of the multiparous females studied did not influence either the proportion of the females retrieving and holding or the character of the responses shown to neonates (Table 2). As long as females were multiparous, their responses to neonates were similar regardless of whether they were intact and cycling, ovariectomized, or relatively old and menopausal. Statistically significant differences among these types were not found for any of the behavioral measures studied. Pregnancy and parturition appeared to be powerful factors altering the characteristic response of young females from indifference to intense maternalness. Six laboratory-reared females (average age, 4.9 years) were observed within 10 days after their first parturition. All behaved toward their own infants quite like the multiparous females with their “adopted” infants. The primiparous females held their infants ventroventrally nearly continuously while being watched, groomed them, and restrained the infants when they attempted leaving.
MATERNAL
Responses of Multiparous
353
RESPONSES TO RHESUS INFANTS TABLE 2 Rhesus Females Varying in Endocrine State to Unfamiliar Neonates Type of multipare (N) INTACT
Response % retrieving % holding ventroventrai Latency (min) to retrieve Latency (min) to touch Ventroventral
holding (frequencyy
AID <60 cm (frequency) AID >60 cm (frequency)
(7)
85.7 85.7 0.25 (0.25-240) 0.25 (0.25- 1.O) 237 (o-240) 240 ( 128-240) 1 (o-203)
OVX (6) 83.3 83.3 0.25 (0.25-240) 0.37 (0.25-3.50) 232 (o-240) 240 (208-240) 2 (O-28) (2?90)
100 100 0.25 (cO.25) 0.25 (~0.25) 229 (17-240) 237 (223-240) 12 (O-57) 8 (2-19)
(LO)
O-35)
Touching (frequency) Grooming (frequency)
:04_45) 34 (O-45)
MENOP (6)
LI Frequency measures are based on the number of IS-set intervals during which the response was recorded. Data in the table show the median of individual medians with ranges in parentheses.
Mammary Responses
Preceding exposure to infants, no fluid was able to be exuded by palpation from the nipples of the experimental females. The nipples of these animals, particularly the OVX and MENOP groups, appeared undeveloped and with little coloration. Unexpectedly, after five I-hr exposure periods to infants, small amounts of fluid could be expressed from the nipples of 15 of 17 females that retrieved and held infants, henceforth referred to as “adopters.” In contrast, the nipples of 8 females that remained indifferent to infants (“nonadopters”) were completely dry. These simple tests for expressibility of fluid were conducted approximately 1 hr after the fifth test. However, 3 out of 4 adopting females examined 24 hr after their first behavioral test, that is, after only 1 hr of contact with an infant, were producing secretions. Many of the infants picked up and positioned by the female were observed to be mouthing and sucking on her nipples during the I-hr test. However, a mechanical sucking stimulus was not necessarily required for the initiation of liquid secretion, and certain females whose nipples were never contacted by infants in any test nevertheless produced fluid from their nipples at the conclusion of these five tests (Table 3).
354
HOLMAN
AND COY
TABLE 3 Mammary Responses Shown by Adult Rhesus Females
Female group INTACT ovx MENOP
Median nipple length (range) 1.05 (0.5-2.1) (OYO.9) 0.71 (0.3-0.9)
Proportion of adopters secreting fluid
Number secreting without nipple contact from infant
516
-
415
1
6l6
3
Median score of fluid consistency Ow3eY 2.5 (2-4) 3 (2-4) 1
(1-2)
a Fluid consistencies were loosely categorized as: thin, colorless liquid = 1; white liquid, resembling skimmed milk = 2; thick white liquid = 3.
At the conclusion of behavioral testing secretory products of individual adopting females showed all of the stages described previously. It was usually the case that of the three multiparous groups a higher number of INTACT females produced the thicker, more substantial-looking fluid whereas the liquid from females in the OVX and MENOP groups appeared thin and watery (Table 3). Nonetheless, our use of this color-coding system should not be taken to imply that the secretions were identical to rhesus milk. Although the fluid expressed from the adopting females’ nipples resembled milk, in preliminary studies, four females that had continuously lived with infants up to 14 days were never able to nurture the infant completely. Their infants lost weight, showed signs of dehydration, and required supplementary feedings from nursing bottles. DISCUSSION Practically all multiparous females responded immediately to the young infants with a seemingly complete display of maternal behavior in contrast to the nulliparous females that displayed very few maternal patterns toward infants. Presenting infants to nonadopting females for five I-hr periods or, on occasion, extending this exposure for even longer periods, did not lead to an eventual increase in the amount of maternal behavior. In several species of rodents, presentation of neonates for 1 to 7 days (a process referred to as priming or concaveation) eventually stimulated even virgin females to display maternal responsiveness (Noirot, 1964; Richards, 1966; Rosenblatt, 1%7). We were unable to obtain comparable priming in rhesus. In rodents maternal responsiveness can be facilitated by various hormonal treatments (Terkel and Rosenblatt, 1968; Moltz, Lubin, Leon, and
MATERNAL
RESPONSES TO RHESUS INFANTS
355
Numan, 1970; Krehbiel and LeRoy, 1979). We found no evidence for ovarian influences on multiparous rhesus adoption. Hormonal facilitation of maternal behavior in nulliparous females was not investigated in the present study. It can be suggested, however, that during parturition alterations in hormone levels in nulliparous females are able to induce or facilitate activation of mechanisms underlying behavior. The question of whether oxytocin (Klopfer and Klopfer, 1968; Pederson and Prange, 1979) has any special role in the process bears investigation. Although parity is suggested to be the major factor influencing maternal behavior, age and, in particular, social rearing also differed between the nulliparous and multiparous groups and could be instrumental in the development of activational mechanisms underlying maternal adoption. The nulliparous females were reared in the laboratory with mothers and peers only, so that, unlike the feral-reared, multiparous females, they were disadvantaged by not being able to interact with infants and younger animals during their own development. Such interactions, it has been argued, benefit the display of infant caretaking at maturity (Gartlan, 1969; Lancaster, 1971; Blaffer-Hrdy, 1976; Clutton-Brock and Harvey, 1976). We wish to draw attention to the fact, however, that in our small sample of laboratory-reared primiparous females, all consistently showed strong attachment and caretaking behaviors with their own first born, although they were not observed under experimental conditions. A learning or imprinting-like process of mothering seems to occur, therefore, around parturition in first-time mothers. This developmental process might well be dependent on hormones, but might also be presensitized for later activation in rhesus monkeys through interactions with infants and neonates during their prepubertal lives. An especially interesting observation was the fluid exuded from adopting females’ nipples, particularly in the absence of direct physical stimulation by the infant of the nipples. It was probably not the case that manipulation of the nipples during examination helped stimulate fluid secretion in the multiparous females as in three cases fluid could be expressed during the first examination. We were not able to distinguish between secretion of fluid that was already present in the mammary ducts (let down) and new production of fluid (Schams, 1976). It can be implied, nevertheless, that in some individual animals, since the fluid became more opaque and thicker as the number of behavioral tests increased, the cells in the mammary glands were metabolically active. Whether any of the adopting females would, in time, be able to produce sufficient amounts of nutritious fluid for the complete sustenance of an infant was a question we were not able to examine adequately. ACKNOWLEDGMENTS We thank Drs. J. A. Robinson and W. E. Bridson for furnishing assays on the postmenopausal female group. This research was supported by Grants MH21312 from the
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AND GOY
National Institute of Mental Health to R. W. Goy and RR00167 from the National Institutes of Health to the Wisconsin Regional Primate Research Center. Publication 20-020 of the Wisconsin Regional Primate Research Center.
REFERENCES Blaffer-Hrdy, S. (1976). Care and exploitation of nonhuman primate infants by conspecifics other than the mother. Advan. Study Behav. 6, 101-158. Bullerman, R. (1950). Notes on kidnapping by bonnet monkeys. J. Mammal. 31, 93-94. Clutton-Brock, T. H., and Harvey, P. H. (1976). Evolutionary rules and primate societies. In P. P. G. Bateson and R. A. Hinde (Eds.), Growing Poinrs in Ethology, pp. 195-238. Cambridge Univ. Press, London/New York. Deets, A. C., and Harlow, H. F. (1974). Adoption of single and multiple infants by rhesus monkey mothers. Primates 15, 193-203. Gartlan, J. S. (1%9). Sexual and maternal behavior of the vervet monkey, Cercopirhecus aethiops. J. Reprod. Fertil. Suppl. 6, 137-150. Hansen, E. W. (1966). The development of maternal and infant behavior in the rhesus monkey. Behaviour 27, 107-149. Harlow, H. F., Harlow, M. K., and Hansen, E. W. (1%3). The maternal affectional system of rhesus monkeys. In H. L. Rheingold (Ed.), Maternal Behavior in Mammals, pp. 254-281. Wiley, New York. Hinde, R. A. (1%5). Rhesus monkey aunts. In B. M. Foss (Ed.), Determinants ofInfant Behaviour, Vol. 3, pp. 67-71. Methuen, London. Holman, S. D., Yoshihara, D. L., and Goy, R. W. Interactions between infant and other troop members in a captive group of wild-caught rhesus monkeys. Submitted to J. Znr. Primatol. Jay, P. C. (1962). Aspects of maternal behavior among Langurs. Ann. N. Y. Acad. Sci. 102, 468-476.
Klopfer, P. H., and Klopfer, M. S. (1%8). Maternal “imprinting” in goats: Fostering of alien young. Z. Tierpsychol. 25, 862-866. Krehbiel, D. A., and LeRoy, L. M. (1979). The quality of hormonally stimulated maternal behavior in ovariectomized rats. Harm. Behav. 12, 243-252. Lancaster, J. B. (1971). Play-mothering: The relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol. 15, 161-182. Marsden, N. M., and Vessey, S. H. (1%8). Adoption of an infant green monkey within a social group. Commun. Behav. Biol. A 2, 275-279. Moltz, H., Lubin, M., Leon, M., and Numan, M. (1970). Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol. Behav. 5, 1373-1377. Noirot, E. (1964). Changes in responsiveness to young in the adult mouse. II. The effect of external stimuli. J. Camp. Physiol. Psychol. 57, 97-99. Pedersen, C. A., and Prange, A. J., Jr. (1979). Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Nat. Acad. Sci. USA 76, 6661-6665. Quiatt, D. (1977). Aunts and mothers: Adaptive implications of allomaternal behavior of nonhuman primates. Amer. Anfhropol. 81, 3 10-3 19. Richards, M. P. (1966). Maternal behaviour in the golden hamster: Responsiveness to young in virgin, pregnant and lactating females. Anim. Behav. 14, 310-313. Rosenblatt, J. S. (1967). Nonhormonal basis of maternal behavior in the rat. Science 156, 1512-1514. Rosenblum, L. A. (1971). Infant attachment in monkeys. In H. R. Schaffer (Ed.), The Origins of Human Social Relations, pp. 85-l 13. Academic Press, New York. Rosenblum, L. A. (1972). Sex and age differences in response to infant squirrel monkeys. Brain Behav. Evol. 5, 30-40.
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Rowell, T. E., Hinde, R. A., and Spencer-Booth, Y. (1964). “Aunt”-infant interaction in captive rhesus monkeys. Anim. Behav. 12, 219-226. Schams, D. (1976). Hormonal control of lactation. In Breast-Feeding and the Mofher, pp. 27-48. Ciba Foundation Symposium, Vol. 45, Elsevier Excerpta Medica NorthHolland, Amsterdam. Seay, B. (1966). Maternal behavior in primiparous and multiparous rhesus monkeys. Folia Primatol. 4, 146-168. Sugiyama, Y. (1965). Behavioral development and social structure in two troop of Hanuman Langurs (Presbytis entellus). Primates 6, 213-247. Terkel, J., and Rosenblatt, J. S. (1%8). Maternal behavior induced by maternal blood plasma injected into virgin rats. J. Comp. Physiol. Psychol. 65, 479-482. van Wulfften, Pahhe, T., and van Hoof, J. A. R. A. M. (1975). A case ofthe adoption of an infant chimpanzee by a suckling foster chimpanzee. Primates 16, 231-234. Welker, C. (1977). Adoptionen bei Macaca fascicularis. Verb. Deut. Zool. Ges 70, 338.
AND
Behavioral
BEHAVIOR
14, 348-357 (1980)
and Mammary Responses of Adult Female Rhesus to Strange Infants S.D.
HOLMAN AND R. W.Gou
Wisconsin Regional Primate Research Center, University of Wisconsin, 1223 Capitol Court, Madison, Wisconsin 53706 Approximately 90% of gonadally intact, ovariectomized, or postmenopausal feral-born multiparous rhesus macaques immediately behaved maternally and displayed strong attachment to unfamiliar neonatal rhesus infants offered to them, even though the females had not lived with infants for at least 12 months. Females showing such behavior and attachment also showed fluid secretion from their nipples even, in some cases, without oral stimulation of the nipples by the infant. Adult laboratory-reared nulliparous females did not adopt infants, although identically reared primiparous females adequately cared for their own first infants.
In natural troops or groups living in laboratories, female primates occasionally permanently adopt solitary young infants (Hinde, 1965; Marsden and Vessey, 1968; van Wulfften Palthe, and van Hoof, 1975; Welker, 1977) or kidnap infants not allowing their natural mothers to retrieve them (Bullerman, 1950; Rosenblum, 1971; Quiatt, 1977). Although adoptions may not always save the solitary infant and kidnappings work to the infant’s disadvantage, the occurrence of these activities reflects the value of the infant as an object for possession by young and adult females (Jay, 1962; Sugiyama, 1965; Lancaster, 1971; Rosenblum, 1972). During the early birth season, young nulliparous female rhesus macaques living in social groups are often observed touching, grooming (Rowell, Hinde, and Spencer-Booth, 1964), holding ventroventrally, and carrying infants (Holman, Yoshihara, and Goy in preparation). In a more experimental situation, Rosenblum (1972) has found that full-term pregnant squirrel monkeys, as well as immature females, retrieve “abandoned” infants more frequently than do other age/sex classes. Multiparous rhesus monkeys, whose infants had been removed within a few hours after birth, readily accepted and cared for another female’s newborn when it was presented to them within a few days of their own parturition (Deets and Harlow, 1974). Unexamined in that study, however, is the question of whether recent parturition and the presence of ovarian hormones are crucial for the facilitation of maternal behavior. 348 0018-506X/80/040348-10$01.00/0 Copyright @ 1980 by Academic Press, Inc. All rights of reproduction in any form reserved.
MATERNAL
RESPONSES
TO RHESUS
INFANTS
349
This report provides a description of the phenomenon of adoption experimentally evoked in adult female rhesus monkeys (Mucaca mulatta) housed alone for at least 12 months, and examines the influence of parity, rearing, and ovarian hormones on this behavioral response. METHODS Subjects Experimental females. Twenty-five mature female rhesus monkeys were classified into one nulliparous and three multiparous groups. The feral-born multiparous monkeys consisted of females (INTACT; mean age, 15.6 years) that had regular menstrual cycles (N = 7), females )OVX; mean age, 18.9 years) whose ovaries had been removed at least 19 months previously (N = 6), and aged females (MENOP; mean age estimated to be greater than 25 years) that had ceased having regular menstrual cycles at least 32 months previously (N = 6). Females in this last category were judged to be postmenopausal as in all cases a IZmonth period had elpased without menstrual bleeding. Hormonally, these females were similar to ovariectomized females with high gonadotropins and low estradiol and progesterone levels (Robinson and Bridson, personal communication). The nulliparous group, laboratory born and reared (NULLIP; mean age, 7.1 years) had regular menstrual cycles. All 25 females had been housed alone for at least 14 months, with a mean value of 67.4 months. It is important to point out that the nulliparous females used in this study were not reared in social isolation. For the first year of life they lived continuously in small groups consisting of their own mothers and four or five other mothers and infants of both sexes. They were weaned at 1 year of age and from then on lived continuously with the age-mates they had lived with during the first year except for short periods when they were separated for purposes of behavioral study. Thus these females were not socially deprived except in the sense that the composition of their social group was not as complex as that usually prevailing for feral animals. A second group of females (PRIMIP; mean age, 4.9 years, N = 6) took part in this study. These were females that had been born and reared in the laboratory and had recently given birth to their first infant. This group was not manipulated in any way. The females were housed in single cages under a 12-12 light cycle. Purina Monkey Chow was made available each morning with fresh fruit supplementing this diet occasionally. Water was continuously available. Experimental infants. Forty-three infants, aged between 2 and 12 days, were used as stimulus animals in the behavioral tests. As the infant physically matures and its movements become coordinated, its behavioral role in the regulation of the infant/experimental female interaction becomes more important. Although in this study the infants used were as young and immature as possible, some experimental females had to be
350
HOLMANANDGOY
quite active in keeping some of the struggling position.
infants in a ventroventral
PROCEDURE
Each experimental female (from groups INTACT, OVX, MENOP, AND NULLIP) was housed in the behavioral testing cage (0.75 x 1.5 x I. 15 m high) approximately 24 hr before the adoption tests began. The female was removed from the cage, a strange infant placed in the cage, and the female allowed to return. The duration of the test was 1 hr, after which the infant was removed. Such tests were given to each female on 5 separate days. Tests were occasionally extended, particularly in those cases where the female’s maternal responses were minimal (two multiparous females and three nulliparous females). Scheduling of tests depended on the availability of infants, but, on average, all five tests for a given female were completed within 7 days. The experimental females were presented with one male and one female infant; some females were presented with a different infant in each test. Before, intermittently, during, and after the behavioral testing series each female was examined for secretions from her nipples. This was carried out by manually palpating the area around the nipple and then gently squeezing the nipple. This simple procedure proved adequate for exuding any fluid present in the mammary ducts. Since in most cases the volume of nipple fluid produced was too small to analyze its constituents biochemically, a color coding system, which has been used to grade the quality of rhesus’ milk, was used. Immediately following weaning, milk in rhesus mothers runs through a number of consistency stages starting as a thick white liquid (fluid consistency score = 3) and ending 3 or 4 days later as a thin watery liquid (fluid consistency score = 1). Milk production ceases soon after this final stage (personal observation). The PRIMIP females were observed in their home cages for 1 hr with their own infants beginning a few days after they had given birth. Five such observations were carried out on 5 subsequent days. Behavior
Patterns
and Their Measurement
A check sheet, divided into 15-set intervals, was used to record behavior during the tests (groups, INTACT, OVX, MENOP, and NULLIP) as well as during the hour-long observations of the primiparous females. Each behavior was recorded only once during each interval regardless of the frequency with which it was displayed during that interval. The behavioral criteria (described below) used to define maternally related behavior were established from pilot studies and from published material on rhesus maternal behavior (Harlow, Harlow, and Hansen, 1963; Hansen, 1966; Seay, 1966). Approach. Animal (infant or female) approaches partner to within 60 cm.
MATERNAL
RESPONSES
351
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Leave. Animal moves at least 60 cm away from partner. Animal interdistance (AID). The frequency of 15set intervals or parts of 1%set intervals that the animal was under (AID < 60) or over (AID > 60) 60 cm. Lipsmack. Adult female moves lips rapidly in a kissing fashion with smacking sounds. The female’s head is usually turned toward infant. This behavior pattern is thought to be a nonhostile, friendly gesture although it is often seen in what seem to be contexts of mild apprehension. Groom. Female grooms infant’s pelage; the fur on the infant’s back or around its genital area is usually groomed. The female often lipsmacks during initiation of grooming. Touch. The female physically handles and manipulates the infant, for example, during visual examination and inspection of the infant. Restrain. Whether or not the female had to be physically restrained while the infant was forcibly removed at the end of the test was recorded. For some of the behavioral patterns latency was estimated to the nearest 15set interval from beginning of the test to the occurrence of the particular response. Statistical analyses were performed on the medians of the median frequencies for behavioLs. RESULTS
Behavioral Responses The major factor affecting the nature of the responses shown by adult females toward the infants was prior parity (Table 1). Seventeen of the nineteen multiparous females tested retrieved and held the infant in a ventroventral position, and they did so on all five tests. Nulliparous females never retrieved or held the infant ventroventrally. Similarly, the two multiparous females that failed to pick up and hold the infants offered behaved consistently on all five tests. As shown in Table 1 all multiparous females that retrieved and held the infant had to be physically restrained at the end of the test and the infant was forcibly removed. This procedure was unnecessary with any of the nulliparous females. No multiparous female that held an infant ever abandoned that infant when the test ended and the female reentered the transport box. When she did so, she carried Responses of Multiparous
Response % Retrieving % Holding ventroventral % Restrained
TABLE 1 and Mulliparous Adult Rhesus Females to Unfamiliar Neonates Nulliparous (N = 6) 0 0 0
Multiparous (all types combined N = 19) 89.5 89.5 89.5
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the infant with her. In short, for these three types of behavioral events (retrieving, holding, and the need for physical restraint to affect separation) the females tested responded in an all-or-none fashion and their pattern of response was consistent from test to test. The failure to respond positively toward an infant was a conspicuously consistent trait of some females. The one nulliparous and two multiparous females that failed to retrieve or hold infants in the standardized test were allowed to live continuously for 10 days with a bottle-fed infant. Throughout this period, they never held the infant during the hour-long daily observation. In addition, two nulliparous females were tested daily in 2-hr sessions for 10 days. Neither ever retrieved or held the infants. Neither in the special circumstances described in the preceding paragraph nor in the standardized tests were hostile responses toward the infants shown by females failing to retrieve and hold. Characteristically, such females were indifferent to the infants offered. Occasionally during the standardized tests, however, some affiliative responses to the infants were shown by nulliparous females. For example, nulliparous females sat near the infant (AID < 60 cm) during 69 of the possible 240 15-set intervals on average (range of individual medians over the five tests was 24 to 150 15-set intervals). But multiparous females were within 60 cm of the infant during 240 15-set intervals on average (range 128-240, Mann-Whitney U = 112.0, P < 0.002). Grooming the infant was observed during a maximum of five 15-set intervals (overall median = 0) for nulliparous compared with a median of 18 intervals (range 0 to 80) for multiparous females (U = 103.5, P < 0.002). Touching the infant, while not frequent among nulliparous females (median 0, range 0 to 27), occurred during nineteen 15-set intervals on average for multiparous females (range 0 to 90, U = 99.0, P < 0.01). Lipsmacking was the only response displayed nearly equally often by nulliparous (median = 7, range I to 28) and multiparous (median = 10, range 5 to 92) females. The variations in endocrine status of the multiparous females studied did not influence either the proportion of the females retrieving and holding or the character of the responses shown to neonates (Table 2). As long as females were multiparous, their responses to neonates were similar regardless of whether they were intact and cycling, ovariectomized, or relatively old and menopausal. Statistically significant differences among these types were not found for any of the behavioral measures studied. Pregnancy and parturition appeared to be powerful factors altering the characteristic response of young females from indifference to intense maternalness. Six laboratory-reared females (average age, 4.9 years) were observed within 10 days after their first parturition. All behaved toward their own infants quite like the multiparous females with their “adopted” infants. The primiparous females held their infants ventroventrally nearly continuously while being watched, groomed them, and restrained the infants when they attempted leaving.
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RESPONSES TO RHESUS INFANTS TABLE 2 Rhesus Females Varying in Endocrine State to Unfamiliar Neonates Type of multipare (N) INTACT
Response % retrieving % holding ventroventrai Latency (min) to retrieve Latency (min) to touch Ventroventral
holding (frequencyy
AID <60 cm (frequency) AID >60 cm (frequency)
(7)
85.7 85.7 0.25 (0.25-240) 0.25 (0.25- 1.O) 237 (o-240) 240 ( 128-240) 1 (o-203)
OVX (6) 83.3 83.3 0.25 (0.25-240) 0.37 (0.25-3.50) 232 (o-240) 240 (208-240) 2 (O-28) (2?90)
100 100 0.25 (cO.25) 0.25 (~0.25) 229 (17-240) 237 (223-240) 12 (O-57) 8 (2-19)
(LO)
O-35)
Touching (frequency) Grooming (frequency)
:04_45) 34 (O-45)
MENOP (6)
LI Frequency measures are based on the number of IS-set intervals during which the response was recorded. Data in the table show the median of individual medians with ranges in parentheses.
Mammary Responses
Preceding exposure to infants, no fluid was able to be exuded by palpation from the nipples of the experimental females. The nipples of these animals, particularly the OVX and MENOP groups, appeared undeveloped and with little coloration. Unexpectedly, after five I-hr exposure periods to infants, small amounts of fluid could be expressed from the nipples of 15 of 17 females that retrieved and held infants, henceforth referred to as “adopters.” In contrast, the nipples of 8 females that remained indifferent to infants (“nonadopters”) were completely dry. These simple tests for expressibility of fluid were conducted approximately 1 hr after the fifth test. However, 3 out of 4 adopting females examined 24 hr after their first behavioral test, that is, after only 1 hr of contact with an infant, were producing secretions. Many of the infants picked up and positioned by the female were observed to be mouthing and sucking on her nipples during the I-hr test. However, a mechanical sucking stimulus was not necessarily required for the initiation of liquid secretion, and certain females whose nipples were never contacted by infants in any test nevertheless produced fluid from their nipples at the conclusion of these five tests (Table 3).
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TABLE 3 Mammary Responses Shown by Adult Rhesus Females
Female group INTACT ovx MENOP
Median nipple length (range) 1.05 (0.5-2.1) (OYO.9) 0.71 (0.3-0.9)
Proportion of adopters secreting fluid
Number secreting without nipple contact from infant
516
-
415
1
6l6
3
Median score of fluid consistency Ow3eY 2.5 (2-4) 3 (2-4) 1
(1-2)
a Fluid consistencies were loosely categorized as: thin, colorless liquid = 1; white liquid, resembling skimmed milk = 2; thick white liquid = 3.
At the conclusion of behavioral testing secretory products of individual adopting females showed all of the stages described previously. It was usually the case that of the three multiparous groups a higher number of INTACT females produced the thicker, more substantial-looking fluid whereas the liquid from females in the OVX and MENOP groups appeared thin and watery (Table 3). Nonetheless, our use of this color-coding system should not be taken to imply that the secretions were identical to rhesus milk. Although the fluid expressed from the adopting females’ nipples resembled milk, in preliminary studies, four females that had continuously lived with infants up to 14 days were never able to nurture the infant completely. Their infants lost weight, showed signs of dehydration, and required supplementary feedings from nursing bottles. DISCUSSION Practically all multiparous females responded immediately to the young infants with a seemingly complete display of maternal behavior in contrast to the nulliparous females that displayed very few maternal patterns toward infants. Presenting infants to nonadopting females for five I-hr periods or, on occasion, extending this exposure for even longer periods, did not lead to an eventual increase in the amount of maternal behavior. In several species of rodents, presentation of neonates for 1 to 7 days (a process referred to as priming or concaveation) eventually stimulated even virgin females to display maternal responsiveness (Noirot, 1964; Richards, 1966; Rosenblatt, 1%7). We were unable to obtain comparable priming in rhesus. In rodents maternal responsiveness can be facilitated by various hormonal treatments (Terkel and Rosenblatt, 1968; Moltz, Lubin, Leon, and
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Numan, 1970; Krehbiel and LeRoy, 1979). We found no evidence for ovarian influences on multiparous rhesus adoption. Hormonal facilitation of maternal behavior in nulliparous females was not investigated in the present study. It can be suggested, however, that during parturition alterations in hormone levels in nulliparous females are able to induce or facilitate activation of mechanisms underlying behavior. The question of whether oxytocin (Klopfer and Klopfer, 1968; Pederson and Prange, 1979) has any special role in the process bears investigation. Although parity is suggested to be the major factor influencing maternal behavior, age and, in particular, social rearing also differed between the nulliparous and multiparous groups and could be instrumental in the development of activational mechanisms underlying maternal adoption. The nulliparous females were reared in the laboratory with mothers and peers only, so that, unlike the feral-reared, multiparous females, they were disadvantaged by not being able to interact with infants and younger animals during their own development. Such interactions, it has been argued, benefit the display of infant caretaking at maturity (Gartlan, 1969; Lancaster, 1971; Blaffer-Hrdy, 1976; Clutton-Brock and Harvey, 1976). We wish to draw attention to the fact, however, that in our small sample of laboratory-reared primiparous females, all consistently showed strong attachment and caretaking behaviors with their own first born, although they were not observed under experimental conditions. A learning or imprinting-like process of mothering seems to occur, therefore, around parturition in first-time mothers. This developmental process might well be dependent on hormones, but might also be presensitized for later activation in rhesus monkeys through interactions with infants and neonates during their prepubertal lives. An especially interesting observation was the fluid exuded from adopting females’ nipples, particularly in the absence of direct physical stimulation by the infant of the nipples. It was probably not the case that manipulation of the nipples during examination helped stimulate fluid secretion in the multiparous females as in three cases fluid could be expressed during the first examination. We were not able to distinguish between secretion of fluid that was already present in the mammary ducts (let down) and new production of fluid (Schams, 1976). It can be implied, nevertheless, that in some individual animals, since the fluid became more opaque and thicker as the number of behavioral tests increased, the cells in the mammary glands were metabolically active. Whether any of the adopting females would, in time, be able to produce sufficient amounts of nutritious fluid for the complete sustenance of an infant was a question we were not able to examine adequately. ACKNOWLEDGMENTS We thank Drs. J. A. Robinson and W. E. Bridson for furnishing assays on the postmenopausal female group. This research was supported by Grants MH21312 from the
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National Institute of Mental Health to R. W. Goy and RR00167 from the National Institutes of Health to the Wisconsin Regional Primate Research Center. Publication 20-020 of the Wisconsin Regional Primate Research Center.
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