Further hormonal suppression of eldest daughter cotton-top tamarins following birth of infants.код для вставкиСкачать
American Journal of Primatology 31:ll-21 (1993) Further Hormonal Suppression of Eldest Daughter Cotton-Top Tamarins Following Birth of Infants CHARLES T. SNOWDON, TONI E. ZIEGLER, AND TINA M. WIDOWSKI Department of Psychology and Wisconsin Regional Primate Center, University of Wisconsin, Madison Reproductive suppression of females is found throughout the Callitrichids. However, in many species some evidence of ovarian activity is observed in subordinate females. Subordinate cotton-top tamarin females in our colony have never been observed to ovulate in the presence of a reproductive female. However, ovarian follicular development does occur, and measurable levels of urinary estrogen and luteinizing hormone are frequently found in subordinate females. We studied 11 female tamarins living in family groups with a reproductive female. Each of the 8 eldest daughters had measurable urinary estrogen and LH levels and showed a reduction of hormonal levels when new infants were born. The 3 younger daughters showed barely detectable hormonal levels that did not change. Following the birth of infants the eldest daughters scent marked less frequently, increased time in contact with and grooming group members other than the mother, but they were more often targets of aggression than immediately prior to infant births. The eldest daughters were somewhat less involved in care of new infants than expected, although they spent much time in proximity to those carrying the infants. These results suggest that the further reduction of hormonal levels in subordinate females after the birth of infants may function to prevent these females from competing with mothers during the post-partum estrus rather than recruiting the eldest daughters as helpers for infant care. o 1993 Wiley-Liss, Inc. Key words: reproductive suppression, parturition, infant care, estrogen, luteinizing hormone, aggression, scent marking, social behavior INTRODUCTION The Callitrichidae are characterized by a cooperative breeding system where one female breeds while other group members assist with the care of infants [Goldizen, 1987; Sussmann & Garber, 19871. This allows subordinate helpers within groups to learn parental care skills from helping to care for infants [Epple, 1978; Cleveland & Snowdon, 19841. The adaptiveness of the cooperative breeding system may be explained by the post-partum estrus and conception coupled with Received for publication July 27, 1992;revision accepted February 23,1993. Address reprint requests to Dr. Charles T. Snowdon, Department of Psychology, University of Wisconsin, 1202 West Johnson Street, Madison, WI 53706. 0 1993 Wiley-Liss, Inc. 12 I Snowdon et al. the birth of twins that are 15-25% of the mother’s body weight a t birth which requires the presence of helpers to successfully rear the infants [Snowdon, 19891. Reproductive suppression is critical to the maintenance of a single reproductive female within a group, and such suppression has been often documented among subordinate female Callitrichid monkeys. Newly formed groups of common marmosets (Cullithrix jucchus) quickly result in one female who cycles and becomes reproductive while remaining females in the group are reproductively suppressed [Abbott, 19841. Studies of captive cotton-top tamarins (Suguinus oedipus) have shown that daughters living with a reproductive female do not ovulate [French et al., 1984; Tardif, 1984; Ziegler et al., 1987bl. However, when removed from the presence of their mothers [Tardif, 1984; Heistermann et al., 19891 or removed from their mothers and placed with novel males [French et al., 1984; Savage et al., 1988; Ziegler et al., 1987133, previously non-ovulating females quickly attain reproductive maturity. The primary mechanism for reproductive suppression appears to be olfactory. Transfers of secretions from the reproductive female to a previously nonreproductive daughter from the same group who had been paired with a mate prevented the onset of ovulation in one saddle-back tamarin (Suguinus fuscicollis) [Epple & Katz, 19841 and delayed the onset of ovulation in cotton-top tamarins [Savage et al., 19881and common marmosets [Barrett et al., 19901. In the common marmoset, blockage of the olfactory system of a subordinate female allows ovulation to occur although the female remains behaviorally subordinate [Abbott et al., 19901. In the cotton-top tamarin, but not the common marmoset, stimulation by a novel male is often necessary for ovulation to begin. Daughters removed from a family with a reproductive female and paired with familiar males, failed to ovulate; however, they ovulated quickly when paired with a novel male [Widowski et al., 19901. Females placed in cages adjacent to males, able to see, hear, and smell but not have any physical contact with a novel male, also ovulated [Widowski et al., 19921. Although suppression of ovulation is common among subordinate marmosets and tamarins, the reproductive system is not inactive. Abbott [ 19841reported that one daughter ovulated in up to 50% of the common marmoset family groups he studied, although only one female in a peer group ovulates [Abbott et al., 19901. French and Stribley [19871found peaks of urinary estrogen in golden lion tamarin (Leontopithecus rosuliu) daughters living with their mothers although the overall estrogen levels were lower than those of the reproductive females. Tardif [19841 described plasma progesterone peaks in cotton-top tamarin females living in family groups although these peaks appeared much later than in females who were removed from the family group. Heistermann et al. [19891 reported that the oldest daughters in family groups of cotton-top tamarins rapidly ovulated when the mother was removed. In our laboratory we have found elevated, but non-cyclic, levels of both urinary estrone glucuronide and luteinizing hormone in subordinate female tamarins while living in family groups, generally after 18 months of age [Ziegler et al., 198713; Widowski et al., 19901. There is also histological evidence of ovarian follicular development in suppressed cotton-top tamarin and saddle-back tamarin females, although these follicles appear to become atretic before complete maturation [Mansdotter et al., 1992; Ziegler et al., 1990al. We have monitored the hormonal levels of reproductively suppressed females for many years. We have previously reported elevated, but non-cycling hormonal levels in one pair of reproductively suppressed twin daughters where the hormonal levels dropped dramatically following the birth of infants to their mother [Ziegler et al., 1987bl. This paper expands our findings of hormonal decline produced when Hormonal Reduction in Female Cotton-Top Tamarins I 13 new infants are born into the family, and provides behavioral data to help understand the significance of this phenomenon. METHODS Subjects The subjects were 11 subadult females from 5 family groups. They ranged in age from 20-32 months a t the start of observations. Two of the subjects were twin sisters. The rest either had a male twin or were singletons. The subjects were housed in family groups in large enclosures in the Primate Reproduction and Behavior Colony at the Psychology Department of the University of Wisconsin, Madison. Details of cage sizes, housing, and husbandry are found in Snowdon et al. . Procedures General. Prior work [Ziegler et al., 1987al demonstrated that cotton-top tamarins have a gestation length of 183 -+ 4 days. By monitoring the reproductive females in each of the family groups we determined the day of ovulation as indicated by an LH peak with a concurrent elevation in levels of urinary estrone conjugates. Conception was indicated by a sustained rise of chorionic gonadotropin (CG) approximately 19 days following the LH peak. From these data we predicted the date of parturition. Three weeks prior to the predicted delivery date of the mother, we began daily urine collection from the eldest and second eldest daughters in the group, and we began behavioral observations. The hormonal collection and behavioral observations continued for 3 weeks following the birth of infants. Hormonal. The first morning void urine sample was collected nearly each day for each of the subjects. A technician entered the colony room when lights went on in the morning and offered small bits of food to the animal whose sample was needed. When the animal began to urinate, the technician held a polystyrene container under the female and collected the urine samples. Samples were collected both from the daughters and from the mothers. The urine samples were centrifuged and aliquotted into separate tubes for estrone and LH assays and frozen at -20°C until assayed. The details of the assays have been previously reported. To determine estrogen levels we used a radioimmunoassay for measuring estrone glucuronide [Ziegler et al., 1987bl. The assay had an intra-assay coefficient of variation of 3.00%and an inter-assay coefficient of variation of 5.88%. Luteinizing hormonelchorionic gonadotropin was assayed using the heterologous radioimmmunoassay procedures reported by Ziegler et al. [1987al. Due to the depletion of antisera, two different radioimmunoassays were used to measure gonadotropin activity. Samples from 2 females were monitored with an assay using an antiserum developed by Dr. G . D. Niswender (GDN 15). When the supply of this antibody became low, we switched to one provided by Dr. G. D. Hodgen (H-26) developed for rhesus macaques. Duplicate samples were assayed with both antibodies and obtained a correlation of r = 0.975 (n = 32). The intra-assay coefficient of variation for the LH/CG assays using the GDN-15 antibody was 5.02% and the inter-assay coefficient of variation was 8.26% (n = 4). The intra-assay coefficient of variation using the H-26 antibody was 2.19% and the inter-assay coefficient of variation was 9.89% (n = 4). Each urine sample was also assayed for creatinine levels (Cr) using a colorimetric technique [Tietz, 19761 to determine the concentration in urine. All hormonal values were divided by creatinine levels to correct for differences in urine concentration. 14 I Snowdon et al. Behavior. With 6 of the subjects behavioral observations were made three times each week for 30 min sessions using focal animal sampling techniques. Frequencies of aggression given, aggression received, scent marking, sniffing of other animals or a t scent marks, receiving sniffing from others, and durations of contact, grooming, and huddling were recorded. In addition, instantaneous scan samples taken every ten sec were used to estimate the proportion of time that animals were within arm’s length or in contact with other animals, a measure of proximity. For 5 animals scan samples of infant carrying were taken four times each day. At 8 A.M., 10 A.M., noon, and 2 P.M. an observer noted which animals were observed to carry the infants. Analyses. Hormonal and behavioral values were averaged for the 21 days prior to the birth of infants and for the 21 days following birth. Correlated sample two-tailed t-tests were used to evaluate significance of changes in hormones and behavior. RESULTS Hormonal Three of the eleven females had barely detectable levels of E,G (< 0.1 pg/mg Cr) and LH (mean -+ s.d. E,G: 0.03 0.005 pg/mg CR; LH: 5.2 ? 1.56 pg/mg CR). These animals ranged in age from 20-27 months, but each of the three had an older sister present in the group who did have measurable hormonal levels, similar to results reported by Heistermann et al. 119891. These females had very low hormonal levels, and showed no change in levels following the infant births. One of these animals was among the 6 animals on whom behavioral observations were made and we separated her data from the main behavioral analyses, leaving a sample of 5 females for behavioral measures. For the remaining 8 females (each the eldest daughter in their family) the hormonal data were quite clear. Figure 1 illustrates hormonal changes for two of the females. Figure 2 presents the means for all 8 females. There was a significant reduction of both urinary E,G and LH levels after the birth of new infants (E,C t(7) = 4.15, P < 0.01; LH t(7) = 4.13, P < 0.01). Females whose LH levels were assayed with the GDN-15 antibody showed a similar drop in hormone levels to those whose LH levels were assayed using the H-26 antibody. * Behavior Table I shows the means and standard deviations of the behavioral measures with significant changes following the birth of new infants. Eldest daughters scent marked significantly less (t(4) = 5.26, P < 0.011, and they were increasingly targets of aggression after new infants were born (t(4) = 3.42, P < 0.05).However, very little of the aggression received was from the reproductive female (3.5 ? 7.8% of all aggression prior to the birth of new infants and 7.7 * 5.9% after the birth of infants). At the same time eldest daughters spent more time in contact with group members other than the breeding female (t(4) = 3.12, P < 0.05) and they groomed other animals more often (t(4) = 2.91, P < 0.05). Much of this behavior was directed toward those carrying infants. A mean of 50.4 -+ 22.5% of all contact time, 24.6 2 27.8% of grooming time, and 79.2 27.8% of all huddling was with animals carrying infants. The instantaneous scan samples of proximity demonstrated that the eldest daughters increased their proximity to other group members after the birth of infants (t(4) = 4.39, P < 0.021, but there was no change in their proximity to the reproductive female (pre: 4.1 -+ 2.78% of intervals, post: 6.4 -+ 3.4%, t(4) = 0.93, P > 0.1). A mean of 48.2 ? 18.4%of scan samples in arm’s length and 55.2 2 * Hormonal Reduction in Female Cotton-Top Tamarins / 15 Solei 60 10 50 t . E ml a t 40 6 30 J . E 0, 3 E 4 20 2 10 0 -25 0 -20 -15 -10 - 5 0 5 10 15 20 25 Days Kayla t t E . ml 3 5 E Days Fig. 1. Daily urinary estrone conjugates ( 0 )and luteinizing hormone concentrations (01 of two eldest daughter cotton-top tamarins (Solei and Kayla) before and after the birth of infanta to the reproductive female in their group. All hormone levels are divided by urinary creatine (Cr) concentration to control for variations in urine concentration. 14.1%of scan samples in contact were with the carriers of infants. The behavioral data from the one younger daughter who was observed were quite different. She received aggression less frequently after the birth of infants, increased scent mark- 16 I Snowdon et al. Pre-l nfants Post-Infants T .jl-7 100 0 Pre-Infants Post-Infants Pre-Infants Post-Infants Fig. 2. Mean and standard deviation of urinary estrone conjugate concentrations for 8 eldest daughter cottontop tamarins before and after the birth of infanta to the reproductive female (top panel). Mean ? S.D. for LWCG concentration for 2 eldest daughters using the GDN-15 antibody (middle panel) and for 6 eldest daughters using the H-26 antibody (bottom panel). ing, and decreased huddling, contact, and proximity to other animals. There were no significant changes in huddling, aggression given or in sniffing, so these data are not included in Table I. The focal females were observed carrying infants in only 6.6 k 32.% of scan samples, and most of the carrying occurred after the first 2 weeks. These females Hormonal Reduction in Female Cotton-TopTamarins / 17 * TABLE I. Means S.D. for Behavioral Measures Before and After Birth of Infants (n = 5) Behavior Pre-infants Post-infants Aggression received (d30 min) Scent marking (d30 min) Grooming (d30 min) Contact (mid30 min) Proximity to others (% of scans) Proximitv to mother (% of scans) 2.46 2 0.84 2.68 2 1.48 0.46 2 0.23 3.58 2 1.43 14.4 2 3.95 4.1 2 2.78 3.20 2 1.08* 2.08 2 1.35** 1.14 f 0.67* 8.04 ? 1.91* 31.9 2 4.35* 6.4 2 3.40 *P < 0.05;**P< 0.01, two-tailed correlated sample t-test carried infants much less frequently than did mothers and fathers and slightly less than the average carrying time for all other siblings (Fig. 3A). Thus although the focal females appeared to be attracted to those who were carrying infants, they did little direct infant care themselves. Since most of the infant carrying observations involving mothers occurred as animals first awoke in the morning, a second analysis using just the 10 A.M., noon, and 2 P.M. observations is shown in Figure 3B. Although mothers were less involved in infant care (16.3 ? 5.9% of scans) there was very little change in carrying by eldest daughters (7.7 & 4.2% of scans). The major increases in infant care were from fathers and other siblings. DISCUSSION The results of this study show that a further reduction of hormonal activity occurs in pubertal, non-cycling eldest daughter cotton-top tamarins when infants are born into the natal group. Both E,G and LH levels decrease to prepubertal levels after the birth of infants. Furthermore, these eldest daughters are increasingly the recipients of aggression from other family members, display a reduction in scent marking and spend more time in contact and huddling with group members other than the breeding female. The eldest daughters are more often within arm’s length of other group members after the birth of new infants, but they do not show increasing proximity to the reproductive female. These females show a low level of involvement in infant care (less than other siblings), although they are often in proximity to o r in contact with the family members that are carrying infants. There are two possible functional explanations for this further reduction of hormonal activity in eldest daughters. First, reduced hormonal activity in eldest daughters might lead them to be more actively involved in the care of infants. Second, since reproductive females have a post-partum ovulation within 3 -5 weeks of giving birth [Ziegler et al., 1987al with an 85% conception rate in captivity [Ziegler et al., 1990b1,the lower levels of hormones in eldest daughters may prevent them from competing with the reproductive female during her post-partum estrous. The reproductive females in the present study ovulated and conceived 20.8 ? 5.8 days after parturition. Although the eldest daughters are frequently in proximity with those carrying infants, the results of this study give greater support to the second hypothesis. The eldest daughters carried infants infrequently. They were frequently in contact with those who were carrying infants, but the eldest daughters often received aggression from other family members, though not from the mothers. Studies on other species support this interpretation. Koenig and Rothe 119911 reported that an elder daughter was expelled from a group of Callithrix jacchus by the reproductive 18 / Snowdon et al. c A E m c 40 1 1 Mother Mother Father Daughter Siblings Father Daughter Siblings Fig. 3. Mean 2 S.D. percentage of scan samples of infant carrying by mothers, fathers, eldest daughters, and the mean for other siblings. A All scan samples; B all scan samples excluding first waking scan sample. female 6 days after the birth of infants. Ferrari [19881 reported emigrations of an adult male and 3 subordinate adult females from a wild Callithrix flaviceps group at about the time of the reproductive female's conception. Reproductive females may be especially sensitive to potential competitors near the time of conception. Heistermann et al. [19891 found that eldest daughters ovulated very quickly when the reproductive female was removed from family groups of cotton-top tamarins. The mechanism of the further reduction of hormonal levels is unknown. The increased levels of aggression may lead to stress which has been shown in common marmosets to play a major role in reproductive suppression in newly formed peer groups [Abbott et al., 19901. However, olfactory stimuli also may be important for further hormonal suppression [Epple & Katz, 1984; Savage et al., 1988; Abbott et al., 1990; Barrett et al., 19901. French and Snowdon [19811 found that female cotton-top tamarins increased rates of scent marking, but did not increase threat or aggression levels when presented with intruder females. In cotton-top tamarins scents also provide information about the time of ovulation [Ziegler et al., 19933. The reproductive female may be able to use increased rate of scent marking or changes in the quality of the scent mark to induce the further reduction of hormone levels in eldest daughters. Hormonal Reduction in Female Cotton-Top Tamarins / 19 The mechanisms of fertility suppression may differ between marmosets and tamarins. Abbott et al.  have reported inhibition of GnRH release in subordinate common marmosets which is mediated by olfactory cues. In contrast Tardif  reported ovulatory levels of progesterone in daughters living in family groups which she interpreted as indicating ovulation. However, these were followed by an insufficient luteal phase, and the peaks did not occur on a regular, cyclic basis. These results may represent the incomplete suppression of GnRH in some daughters, but not a complete release from suppression (S. Tardif, personal communication). We have found in cotton-top tamarins that urinary LH levels do not always remain at low levels in reproductively suppressed postpubertal females [Ziegler et al., 1987b; Widowski et al., 19921. Peaks of urinary LH often occur without corresponding increases in urinary estrogens. There may be hypothalamic release of GnRH in tamarins and the suppression of fertility appears to be a t the level of the ovary. Histological evidence from Mansdotter et al. [19921 and Ziegler et al. [1990al shows follicular development with follicle cells becoming atretic prior to ovulation indicating some pituitary activity. Perhaps the birth of infants leads to a suppression of hypothalamic release of GnRH, preventing ovulation by blocking the further release of LH. The eldest daughters also reduced their rate of scent marking. We have previously noted a close correlation with scent marking rate and estrogen levels [Ziegler et al., 198713; Savage et al., 19881 so the reduced scent marking may be secondary to the reduced estrogen levels. In addition a reduction in scent marking may prevent the eldest daughter from being attractive to males when the reproductive female is likely to conceive again. Price and McGrew [19911 have surveyed captive colonies for departures from monogamy in cotton-top tamarins and find that groups with more than one pregnant female have been unstable and that in no captive group has more than one female reared offspring successfully. In a long-term field study of cotton-top tamarins more than one pregnant female has been found, but only one female in a group has live offspring (A. Savage and H. Giraldo, personal communication). The olfactory mechanisms of reproductive suppression that appear to work well in captivity may be less effective in the natural habitat so redundant mechanisms of suppression might be needed. The present study demonstrates that some mechanism exists to further reduce the low level of reproductive functioning in eldest daughters when new infants are born and during the first weeks post-partum when the breeding female is most likely to ovulate and conceive again. This would be a more efficient time to block a second female from reproduction than later when a second female is well-advanced in pregnancy. CONCLUSIONS 1. The eldest daughter cotton-top tamarins in a group have low, but detectable levels of urinary E,G and LH, and they display a further reduction of these levels with the birth of new infants to the reproductive female. 2. The eldest daughters are more frequently targets of aggression, have lower rates of scent mark, and spend more time in proximity, contact, and huddling with other group members after the birth of new infants. However, although these eldest daughters are attracted to the proximity of those with infants, these daughters display a low involvement in infant care themselves. 3. The function of the further reduction in hormones appears to prevent eldest daughters from competing with the reproductive female during her post-partum estrous rather than recruiting these eldest daughters as helpers to care for infants. 20 I Snowdon et al. 4. The mechanisms of reproductive suppression in Callitrichids are often imperfect, especially in field conditions, and the secondary reduction in hormonal levels of eldest daughters found with the birth of new infants may function as a back-up system to prevent reproductive competition. ACKNOWLEDGMENTS We thank the many people who have assisted with daily urine collection over the several years of this study and Dan Wittwer and Fritz Wegner for technical assistance with the hormonal assays. Supported by USPHS research grant MH 35,215, a Research Scientist Award MH 00,177 to C.T.S., and funds from the University of Wisconsin Graduate School Research Committee. Support of the assay lab at the Wisconsin Regional Primate Center comes from USPHS RR 00,176. We thank Dr. John Mara of Hills Pet Products for his donation of Zupreem Marmoset Diet. This is publication 32-047 of the Wisconsin Regional Primate Center. We thank the three anonymous reviewers for their very helpful suggestions that have improved this paper. Tina M. Widowski is now at Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada N l G 2W1. REFERENCES Abbott, D.H. Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. 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