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Effects of age lactation and repeated cycles on rhesus monkey copulatory intervals.

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American Journal of Primatology 721-26 (1984)
Effects of Age, Lactation, and Repeated Cycles on Rhesus
Monkey Copulatory Intervals
MARK E. WILSON, MARGARET L. WALKER, AND THOMAS P. GORDON
Yerkes Regaonal Pramate Research Center, Emory Unauersrty,Atlanta
Young, sexually mature female rhesus monkeys copulate on more days prior
to conception than do older females, and this prolonged discrete mating
period is associated with a n earlier rise in serum estradiol prior to the first
ovulation of the breeding season. The influence of repeated ovulatory cycles
and the presence of a suckling infant on the copulatory patterns were
examined in two separate analyses. Extending previous work, young, nulliparous females copulated on more days at the first ovulation of the breeding
season than did older, multiparous females. However, the duration of the
copulatory period a t the second ovulation of the breeding season was similar
and significantly shorter for both age groups. Furthermore, the presence of
a suckling infant did not influence the duration of the mating periods in
adult, multiparous females. The onset of copulatory behavior for all females
was associated with serum estradiol concentrations of approximately 90 pg/
ml, indicating that the age and cycle differences in the duration of the
copulatory periods are due to the time course of serum' estradiol prior to
ovulation. A separate, longitudinal analysis of the duration of the mating
period associated with the first ovulation of three successive breeding seasons indicated that females copulated on more days during their first ovulatory cycle of their first breeding season. These data indicate that the
copulatory interval is longer for females during the first ovulation of the
breeding season, and this pattern is accentuated in young, sexually mature
animals.
Key words: copulation, age, repeated cycles, rhesus monkey
INTRODUCTION
Female rhesus monkeys living in outdoor environments exhibit discrete periods
of copulatory behavior associated with conceptions during the annual mating season
[Lindburg, 1971; Carpenter, 19421. This behavior is related to the hormonal condition of the female [Gordon, 19811, as copulations begin during the follicular phase,
when serum estradiol (Ez) levels rise, and then cease abruptly following ovulation,
when concentrations of serum progesterone increase [Wilson et al, 1982aI. The
duration of this mating period is age-dependent, since young females, a t their first
ovulation, copulate on more days prior to conception than older females [Wilson and
Gordon, 19801, and this longer period of copulation is related to a n earlier rise in
serum Ez [Wilson et al, 1982131. These data indicate that the first ovulation of the
Received December 24, 1983; accepted March 20, 1984
Address reprint requests t o Mark E. Wilson, Yerkes Regional Primate Research Center of Emory University, Field Station, 2409 Collins Hill Road, Laurenceville, GA 30245.
(Q 1984 Alan R. Liss. Inc.
22
Wilson, Walker, and Gordon
breeding season is both behaviorally and physiologically different for young, sexually mature females. Since these age differences were observed at the first ovulation for young females in their first breeding season, it is not known how the mating
pattern changes with subsequent ovulations within the same breeding season or
during the first ovulation of successive breeding seasons.
Further, in the original study, the older female group comprised animals resuming ovulation following parturition and lactation. Since the events of lactation may
have antigonadotropic effects [Plant et al, 1980; Schallenberger et al, 19811, the
observed age differences in serum E2 and copulatory patterns could be accounted for
by lactation in adult females and not by some characteristic of young females. In
order to understand better the influence of age on the hormonal induction of female
sexual behavior, the present study examined the duration of female copulatory
periods during the first and second ovulatory cycles of the breeding season for young,
nulliparous females and older, multiparous females who were either lactating or
nonlactating. Furthermore, a longitudinal analysis of a separate group of females
examined the changes in the duration of the discrete copulatory periods a t the first
ovulation of successive breeding seasons.
METHODS
Female rhesus monkeys (Macaca m ulatta) housed in outdoor compounds served
as subjects. Females lived in social groups containing many adult males, females,
and juveniles. Each outdoor- compound, with a n enclosed area of either 30 m x 30 m
or 38 m x 38 m, had attached indoor quarters. Animals were given commercial
monkey feed twice daily and received a daily supplement of fresh fruit,
Effects of Repeated Cycles and Lactation
The influence of repeated ovulatory cycles and lactation on the duration of
female copulatory periods was examined in 16 animals: five females 3.5 years of age
who had not ovulated previously and 11 multiparous females 5.5-10.5 years of age.
Females were housed with vasectomized males so that pregnancy was prevented.
Collection began in September 1981 prior to the beginning of the breeding
season. At that time, the 11multiparous females were lactating, as evidenced by the
presence of suckling infants born the previous spring. The average age of the infants
at the outset was 4.2 & 0.2 months (n = 11;X 5 SE). Behavioral observations were
made 2 hr per day, 6 days per week through the first two ovulatory cycles of the
breeding season. Observations were begun each day at 0900 hr following feeding. In
the present environment, this sampling protocol provided data on female copulatory
patterns identical to that obtained from all-day, 9-hr sampling (unpublished observations). The 11 multiparous females were observed again the following breeding
season, beginning in September 1982 when they were not lactating. Behavioral data
were collected through the first two ovulatory cycles of this breeding season. During
observational sessions, all occurrences of male-female copulations resulting in ejaculations were recorded. Vaginal swabs were obtained 6 days per week to monitor
menstruation. Blood samples (5 mlj were obtained from unanesthetized animals 2
days per week as described earlier [Walker et al, 19831. Harvested serum was
analyzed by radioimmunoassay for Ez and progesterone [Wilson et al, 1982aI. Ovulation was inferred from sustained elevations in serum levels of progesterone > 2
ng/ml.
Longitudinal Changes in Copulatory Periods
Copulatory behavior of 13 female rhesus monkeys housed with intact males was
examined in three successive breeding seasons, from their first ovulation at 3.5
Copulatory Periods in Female Rhesus
23
years of age to 5.5 years of age. During the second breeding season at 4.5 years of
age, 11of 13 females were lactating; during the third breeding season at 5.5 years
of age, four of the 13 females were lactating. Lactation was again inferred from the
presence of suckling infants born the previous spring. Behavioral observations of
male-female copulatory behavior were collected 2-3 hr per day, 6 days per week
from September through December each year. Only data from the first ovulation of
each breeding season for each female were used. Ovulations were confirmed on the
basis of elevations in serum progesterone > 2 ng/ml, if available, or by backdating
168 days from parturition [van Wagenen, 19721.
Analyses
The duration of the discrete copulatory period, defined by the number of consecutive days a female engaged in copulations, was obtained for each female. All
grouped data were expressed as X 2 SE. DiDTerences in the duration of copulatoiy
behavior or serum Ez levels at the initiation of behavior between age groups and
across ovulatory cycles were evaluated by analysis of variance with repeated measures. Serum E2 concentrations associated with the onsct of copulatory behavior were
determined from the first hormone value following the initiation of behavior. Since
previous data had demonstrated that young females exhibit a longer discrete period
of copulations, specific differences between age groups were evaluated with planned
comparisons [Keppel, 19731. All statistical values having a P < 0.05 were considered
significant.
RESULTS
Effect of Repeated Cycles
Age differences in the duration of copulatory periods were only evident at the
first ovulation of the breeding season. As illustrated in Figure 1, young females
4
I
-20
.
-15
I
-10
-5
2nd Ovulation
Menses
1st Ovulation
4
4
1
1
0
5
.
10&5 -10
-5
I
m
0
5
Days from Copulatory Offset
Cx
Fig. 1. Duration of the copulatory periods
? SE)for both age classes of females at the first and second
ovulation of the breeding season. Data are aligncd to the last day of copulatory behavior (Day 0 ) a1 each
ovulation. Also shown arc thc intcrvcning mcnstruation interval.
24
Wilson, Walker, and Gordon
copulated on more days at the first ovulation (F1,14 = 5.73; P < 0.05). In contrast,
all females copulated for a similar number of days at the second ovulation ( F I J ~<
1.0; P > 0.05). The finding of no age differences during the second ovulation resulted
from a significant reduction in the length of the copulatory period for young females
(F1,4 = 12.4; P < 0.05). In addition, multiparous females showed a significant
reduction in the number of days on which they copulated at the second ovulation of
the breeding season (Fl,lo = 11.4; P < 0.05). Thus, young females were observed to
copulate on more days only during the first ovulatory cycle of the breeding season,
with the duration of the copulatory period a t the second ovulation similar and
significantly reduced for both age groups.
All females began copulatory activity when serum EZ levels reached approximately 90 pgiml. Serum E2 associated with the onset of copulatory behavior was
similar a t the first and second ovulation for both young (1st: 93.4
8.4 and 2nd:
99.9 4.2 pgiml) and multiparous females (1st: 85.4 k 4.8 and 2nd: 92.9 +_ 4.2 pgf
ml). No age (F1,14< 1.0) or repeated cycle ( F 1 , ~ 4 = 1.17) differences in serum E2
concentrations following the onset of copulatory behavior were evident.
Effects of Recent Lactation
A recent lactational period did not influence the duration of the copulatory
intervals for multiparous females. The length of the copulatory period during the
first (12.9 k 1.2 days) and second ovulatory cycles (9.7 5 0.8 days) of the breeding
season for nonlactating females was similar to that observed the previous year
following a recent lactation (Fig. 1; 1st: 12.5 k 1.0 days; 2nd: 8.5 f 1.1days; F1,lo <
1.0). However, as in the previous year, the copulatory period during the second
ovulatory cycle was significantly shorter than the period associated with the first
ovulation (Fl,lO = 6.52; P < 0.05). Also, serum levels of EZwere similar at the outset
of copulatory behavior whether the females were nonlactating (83.4 3.2 pg/ml) or
lactating 85.4 k 4.8 pg/ml; t l o = 0.86).
Longitudinal Changes in Copulatory Periods
When female copulatory periods were examined across successive breeding
seasons, the duration was found to be longest a t initial ovulation. As illustrated in
Table I, the copulatory period associated with the first ovulation of the first breeding
season was significantly longer than the first ovulation of the second or third
breeding season (F124 = 13.80; P < 0.05). The duration of the mating periods during
TABLE I. Mean(& SE) Number of Days on Which Females Copulated
During the First Ovulation of Three Successive Breeding Seasons From
3.5 to 4.5 Years of Age
3.6
A11 females
(n = 13)
Lactating only
Nonlactating only
19.5 a
(+
2.1)
Age category years
4.5
5.5
13.3
12.9
(i1.2)
(+ .8)
12.9
14.3
(i1.4)
(+ 1.1)
n=ll
15.5
(+ 2.5)
n=4
n=2
"Significantly higher compared to successive years, P < 0.05.
12.3
(* 1.1)
n=9
Copulatory Periods in Female Rhesus
25
the second and third breeding seasons was similar (F1,24 < 1.0) and characteristic of
that of other adult females (Fig. 1). Further analysis revealed that those females
who were lactating copulated on a similar number of days compared to nonlactating
females during both the second breeding season a t 4.5 years of age (tll = 0.69) and
the third breeding season a t 5.5 years of age (TI1 = 1.03).
DISCUSSION
The present analysis indicates that previously demonstrated age differences in
the duration of female copulatory periods are limited to the first ovulation of the
breeding season when young females experience their initial ovulation. The length
of subsequent copulatory periods is significantly shorter and does not differ from
that of fully adult females. This is true of the second ovulation of this first breeding
season as well as the first ovulation of the second and subsequent breeding seasons.
Furthermore, although lactation may delay the resumption of ovulations [Walker et
al, 1984; Schallenberger et al, 19811, once the ovulatory process is initiated, the
recent experience of lactation has no influence on the duration of mating periods in
adult females. Thus, the observed differences in the length of copulatory intervals
associated with the first ovulation of the breeding season are age-dependent. In
addition to this age effect, the copulatory period was significantly reduced a t the
second ovulatory cycle of the breeding season for multiparous females as well. Since
females copulate on a similar number of days following the Ez peak at ovulation
regardless of age [Wilson et al, 1982b1, the age and cycle differences observed in the
present study are likely due to a n earlier rise in serum EZprior to first ovulation in
both young and older females. These data thus indicate that the hormonal profile
associated with the first ovulation of the breeding season is characteristically different from that observed in subsequent cycles for both young, nulliparous females and
multiparous females.
Following a period of summer and/or lactational anovulation, the first ovulation
of the breeding season for adult females is characterized by a gradual increase in
basal serum levels of gonadotropins followed by serum Ez, some 20-30 days prior to
ovulation [Walker et al, 19841. Progesterone levels do not rise until about two days
following the E2 peak. Subsequent ovulations during the breeding season [Walker
et al, 19831 are then similar to those observed in regularly cycling, laboratory-housed
females. Typically, a relatively fixed follicular phase of 10-12 days is followed by a
luteal phase of 15-18 days [Wilks et al, 19791. Since female copulatory behavior
[Wilson et a1 1982al or other aspects of female or male sexual behavior [Wallen et
al, 19831 are restricted in the present environment to periods when E2 is greater
than 80-90 pgiml and progesterone is low, the length of the copulatory period of
subsequent ovulations is limited to the 10- to 12-day follicular-periovulatoryphase.
On the other hand, copulatory behavior prior to the first ovulation of the breeding
season begins whenever serum Ea levels exceed 80-90 pg/ml and are not constrained
by the inhibitory influences of progesterone.
Superimposed on the time course of hormone levels between the first and second
ovulation of the breeding season is a developmental effect. The long period of
follicular maturation indicated by elevations in serum E2 is simply enhanced for
young females at their initial ovulation [Wilson et al, 1982133. This suggests that
increases in basal levels of serum gonadotropins begin even earlier in young females
prior to the first ovulation. Furthermore, from analyses done on sheep, i t has been
suggested that the neuroendocrine mechanisms that control the seasonal resumption of ovulation in adults are analogous to those that control the occurrence of first
ovulation a t the completion of puberty [Karsch & Foster, 19811. The present data
would support this hypothesis for rhesus monkeys, since the first ovulation of the
26
Wilson, Walker, and Gordon
breeding season for both young and multiparous females is characterized by an
extended period of elevated EZ levels that is presumably due to a gradual increase
in gonadotropin stimulation. Thus, these data suggest a commonality in the physiological control of puberty onset and the seasonal resumption of ovulation in rhesus
monkeys.
CONCLUSIONS
1. Age differences in the duration of rhesus female copulatory periods are
restricted to the initial ovulation of the first breeding season for young females.
2. Although the copulatory period is longer for young females a t the first
ovulation, the period shortens significantly a t the second ovulation of the breeding
season for both young and older females.
3. A recent lactational period has no influence on the duration of the copulatory
period for adult females.
4. These data suggest a commonality in the physiological control of puberty
onset and seasonal resumption of ovulation in rhesus monkeys.
ACKNOWLEDGMENTS
We thank M.A. Smith for her technical assistance and L. Wright for her editorial
assistance. This work was supported by grants from NIH RR00165 and HD16305
and NSF BNS13181.
REFERENCES
Carpenter, C.R. Sexual behavior of free-ranging rhesus monkeys. JOURNAL OF COMPARATIVE PSYCHOLOGY 33:113-142,
1942.
Gordon, T.P. Reproductive behavior in the
rhesus monkey: Social and endocrine variables. AMERICAN ZOOLOGIST 21:185-195,
1981.
Karsch, F.J.; Foster, D.L. Environmental
control of seasonal breeding: A common f i nal mechanism governing seasonal breeding and sexual maturation, pp 30-53 in
ENVIRONMENTAL FACTORS IN MAMMALIAN REPRODUCTION. D. Gilmore; B.
Cook, eds. Baltimore, University Park
Press, 1981.
Keppel, G. DESIGN AND ANALYSIS: A RESEARCHER'S HANDBOOK. Englewood
Cliffs, N.J., Prentice-Hall, 1973.
Lindburg, D.G. The rhesus monkey in North
India: An ecological and behavioral study,
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Plant, T.M.; Schallenberger, E.; Hess, D.L.;
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van Wagenen, G. Vital statistics from a
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Wallen, K.; Winston, L.A.; Gaventa, S.; Collins, D.C. Sexual initiation by group-living
female rhesus in relation to changes in
ovarian steroids. Abstract presented a t the
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Wilks, J.W.; Hodgen, G.D.; Ross, G.T. Endocrine characteristics of ovulatory and anovulatory menstrual cycles in the rhesus
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