вход по аккаунту


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
Department of Psychology and Wisconsin Regional Primate Center, University of Wisconsin,
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
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.
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.
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
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
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
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.
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
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
- 5
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
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
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)
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.
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
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.
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. [1990] have reported inhibition of GnRH release in subordinate common marmosets which is mediated by olfactory cues. In contrast Tardif
[1984] 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.
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.
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.
Abbott, D.H. Behavioral and physiological
suppression of fertility in subordinate marmoset monkeys. AMERICAN JOURNAL
OF PRIMATOLOGY 6:169-186, 1984.
Abbott, D.H.; George, L.M.; Barrett, J.;
Hodges, J.K.; OByrne, K.T.; Sheffield,
J.W.; Sutherland, I.A.; Chambers, G.R.;
Lunn, S.F.; Ruiz de Elvira, M.-C. Social
control of ovulation in marmoset monkeys:
A neuroendocrine basis for the study of infertility. Pp. 135-158 in SOCIOENDOCRINOLOGY OF PRIMATE REPRODUCTION, T.E. Ziegler, F.B. Bercovitch, eds.
New York, Wiley-Liss, Inc., 1990.
Barrett, J.; Abbott, D.H.; George, L.M. Extension of reproductive suppression by
pheromonal cues in subordinate female
marmoset monkeys, Cullithrix jucchus.
FERTILITY 90:411-418,1990.
Cleveland, J.;Snowdon, C.T. Social development during the first twenty weeks in the
cotton-top tamarin (Suguinus o. oedipus)
ANIMAL BEHAVIOUR 32:432-444,1984.
Epple, G. Reproductive and social behavior
of marmosets with special reference to captive breeding. PRIMATES IN MEDICINE10:50-62, 1978.
Epple, G.; Katz, Y. Social influences on estrogen excretion and ovarian cyclicity in
the saddle-back tamarin (Suguinus fusc ~ c o ~ Z Z S ) . AMERICAN JOURNAL OF PRIMATOLOGY 6:215-227, 1984.
Ferrari, S.F. The behaviour and ecology of
the buffy-headed marmoset (Cullithrixfluuiceps). Unpublished Ph.D. dissertation.
London, University College, 1988.
French, J.A.; Abbott, D.H.; Snowdon, C.T.
The effect of social environment on estro-
gen excretion, scent marking and sociosexual behavior in tamarins (Suguinus
oedipus). AMERICAN JOURNAL OF PRIMATOLOGY 6:155-167, 1984.
French, J.A.; Snowdon, C.T. Sexual dimorphism in response to unfamiliar intruders
in the tamarin Suguinus oedipus. ANIMAL BEHAVIOUR 29:822-829,1981.
French, J.A.; Stribley, J.A. Synchronization
of ovarian cycles between and within social
groups in golden lion tamarins (Leontopithecus rosulzu). AMERICAN JOURNAL
OF PRIMATOLOGY 12:469-478, 1987.
Goldizen, A.W. Tamarins and marmosets:
Communal care of offspring. Pp. 34-43 in
Cheney, R.M. Seyfarth, R.W. Wrangham,
T.T. Struhsaker, eds. Chicago, University
of Chicago Press, 1987.
Heistermann, M.; Kleis, E.; Prove, E.;
Wolters, H.-J. Fertility status, dominance
and scent-marking behavior of familyhoused female cotton-top tamarins (Suguinus oedipus) in the absence of their
mothers. AMERICAN JOURNAL OF PRIMATOLOGY 18:177-189, 1989.
Koenig, A.; Rothe, H. Social relationships
and individual contributions to cooperative
behaviour in captive common marmosets
(Cullithrix jucchus). PRIMATES 32:183195,1991.
Mansdotter, S.; Kuderling, I.; Epple, G. Agerelated changes in ovarian morphology of
the South American tamarin Suguinus
fuscicollis (Callitrichidae). JOURNAL OF
ZOOLOGY (LONDON) 227:239-255,
Price, E.C.; McGrew, W.C. Departures from
monogamy in colonies of captive cotton-top
Hormonal Reduction in Female Cotton-TopTamarins / 21
16-27, 1991.
Savage, A.; Ziegler, T.E.; Snowdon, C.T. Sociosexual development, pair-bond formation, and mechanisms of fertility suppression in female cotton-top tamarins
(Suguinus oedipus oedipus) AMERICAN
Snowdon, C.T. Mechanisms maintaining
monogamy in monkeys. Pp. 225-251 in
ed. Sunderland, MA, Sinauer Associates,
Snowdon, C.T.; Savage, A.; McConnell, P.B.
A breeding colony of cotton-top tamarins
(Suguinus oedipus). LABORATORY ANIMAL SCIENCE 35477-480, 1985.
Sussman, R.W.; Garber, P.A. A new interpretation of the social organization and
mating system of the Callitrichidae. INTERNATIONAL JOURNAL OF PRIMATOLOGY 8:73-92,1987.
Tardif, S.D. Social influences on sexual maturation of female Saguinus oedipus oediP U S . AMERICAN JOURNAL OF PRIMATOLOGY 6:199-209, 1984.
Saunders, 1976.
Widowski, T.M.; Ziegler, T.E.; Elowson,
A.M.; Snowdon, C.T. The role of males in
stimulating reproductive function in female cotton-top tamarins Suguinus 0.oedipus. ANIMAL BEHAVIOUR 40:731-741,
Widowski, T.M.; Porter, T.A.; Ziegler, T.E.;
Snowdon, C.T. The stimulatory effect of
males on the initiation but not the maintenance of ovarian cycling in cotton-top
tamarins (Saguinus oedipus). AMERICAN
Ziegler, T.E.; Bridson, W.E.; Snowdon, C.T.;
Eman, S. Urinary eonadotroDin and estrogen excretion d&ng the postpartum estrous, conception and pregnancy in the cotton-top tamarin (Suguinus oedipus
oedipus). AMERICAN JOURNAL OF PRIMATOLOGY 12:127-140,1987a.
Ziegler, T.E.; Savage, A.; Scheffler, G.;
Snowdon, C.T. The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Suguinus oedipus) under varying social conditions.
Ziegler, T.E.; Snowdon, C.T.; Uno, H. Social
interactions and determinants of ovulation
in tamarins (Suguinus). Pp. 113-134 in
REPRODUCTION. T.E. Ziegler, F.B Bercovitch, eds. New York, Wiley Liss, Inc.,
Ziegler, T.E.; Widowski, T.M.; Larson, M.L.;
Snowdon, C.T. Nursing does affect the duration of the post-partum to ovulation interval in cotton-top tamarins (Suguinus oedipus). JOURNAL OF REPRODUCTION
AND FERTILITY 90:563-570,1990b.
Ziegler, T.E.; Epple, G.; Snowdon, C.T.; Porter, T.A.; Belcher, A.M.; Kuderling, I. Detection of the chemical signals of ovulation
in the cotton-top tamarin (Suguinus oedipus). ANIMAL BEHAVIOUR 45:313-322,
Без категории
Размер файла
701 Кб
infant, top, birth, daughters, eldest, following, suppression, hormonal, tamarins, cotton
Пожаловаться на содержимое документа