AMER. ZOOL.

, 21:185-195 (1981)

Reproductive Behavior in the Rhesus Monkey:

Social and Endocrine Variables1
THOMAS P. GORDON
Yerkes Regional Primate Research Center of Emory University, Atlanta, Georgia 30322

SYNOPSIS. Social groups of rhesus monkeys (Macaca mulatto) living in outdoor environ-
ments exhibit a distinct seasonal mating pattern and female rhesus are observed to be
sexually receptive for discrete periods averaging about 9 days duration. In the laboratory
environment mating occurs throughout the year and, in the pair test, female rhesus are
observed to be sexually receptive through all phases of a menstrual cycle, with a peri-
ovulatory peak in copulatory behavior. The apparent conflict between results from field
and laboratory studies has been difficult to resolve because of methodological limitations

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

inherent in each study environment. Studies conducted on social groups of rhesus mon-
keys housed in outdoor compounds, an environment in which the species typical seasonal
mating pattern is preserved and which allows for concomitant measurement of behavioral
and hormonal variables, provided information about the covariance between female sex-
ual behavior and ovarian cycles. Female copulations were observed only in association
with ovulatory cycles, and were limited to the follicular and peri-ovulatory phases of such
cycles, demonstrating that copulatory behavior in female rhesus monkeys is strongly in-
fluenced by cyclic hormonal variables. The studies also revealed that females tend to
conceive on the first ovulatory cycle of the season, that there was no synchrony of cycles
among the females, and that the best predictor of the timing of ovulation in a particular
female is reproductive outcome in the previous year.

INTRODUCTION
Investigations of the behavioral phe-
nomena associated with reproduction have
constituted one of the oldest and most
fruitful areas in the animal behavior liter-
ature. In recent years, our understanding
of these behavioral phenomena has been
advanced through a broadening of re-
search perspectives to include quantifica-
tion of circulating hormones and the study
of neuroendocrine feedback mechanisms.
As a result, it is currently recognized that
describing the sexual behavior in a partic-
ular species constitutes a mere beginning
of the process of elucidating the significant
elements controlling reproduction.
Among the non-human primates, per-
haps the most frequently studied species
has been the rhesus monkey (Macaca mu-
latto). Reproductive behavior in this species
has been examined extensively both in free
ranging social environments and in the
laboratory setting. Methodological differ-
ences between these two approaches have
led to the accumulation of two distinct, if
1
From the Symposium on Social Signals—Compar- to that observed in free-ranging rhesus,
ative and Endocrine Aspects presented at the Annual
Meeting of the American Society of Zoologists, 27— was correlated with concentrations of ovar-
30 December 1979, at Tampa, Florida.
complementary, bodies of data. Field re-
search, conducted in the natural habitat
and with semi-free-ranging captive popu-
lations, utilizing primarily observational
methods, has produced descriptions of
sexual behavior and of the seasonal and
social variables which influence sexual ac-
tivity. Laboratory studies, typically con-
ducted in a restricted social context (the
pair test) have produced a significant lit-
erature describing cyclic hormonal events
and demonstrating the importance of en-
docrine variables in the control of sexual
behavior.
It has been difficult to achieve a synthe-
sis of the vast accumulation of data relating
to reproduction in the rhesus because of
the differences in approach between the
field and laboratory studies, and because
some aspects of the basic reproductive pat-
tern seem to be altered in the laboratory
environment. In this paper, I will sum-
marize the results of studies conducted in
the last several years on rhesus monkeys
maintained in social groups in an outdoor
compound. In this environment, the pat-
tern of sexual behavior, which was similar
ian hormones and other physiological vari-

185
186 THOMAS P. GORDON

ables. These data, placed in the context of
other findings, have provided a better un-
derstanding of the coordination among
seasonal, social and endocrine variables
which influence patterns of sexual activity
and which are essential to reproductive
success.
Field data
One of the most striking aspects of the
field studies is that direct measurement of
the endocrine variables which influence
seasonal mating activity has not been pos-
sible. For example, because of the absence
of fertile matings outside the breeding sea-
son, it is presumed that rhesus females £
an outdoor environment do not exhibit
ovulatory cycles during the non-mating
season. However, direct evidence on this
question is lacking, as is an understanding

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

reproductive behavior of the rhesus mon- of the environmental and endocrine mech-
key is that the occurrence of fertile mat- anisms which control seasonal mating
ings (and consequently of births) is limited cycles in this species.
to a distinct annual season, despite the fact
that this species also is characterized by the Laboratory data
exhibition of true menstrual cycles. This The earliest studies of the rhesus in the
observation was made beginning with the laboratory provided information on the
first systematic study of rhesus in an out- menstrual cycle and the relationship be-
door environment (Carpenter, 1942) and tween physiological phenomena and ovu-
has subsequently been confirmed for rhe- lation, menstruation, and pregnancy (Cor-
sus living in their natural environment ner, 1923; Allen, 1927; Hartman, 1932).
(Southwick et al, 1961; Neville, 1968; These pioneering investigations and many
Lindburg, 1971), for captive groups main- which have followed, provided descriptive
tained on islands (Altmann, 1962; Cona- data and a basic understanding of the na-
way and Koford, 1964; Vandenbergh and ture, timing, and variability in the occur-
Vessey, 1968), and recently for groups rence of ovulatory cycles and related re-
maintained in outdoor compounds (Gor- productive phenomena. Although some
don et al., 1976; Bernstein and Gordon, differences have been observed from
1977; Wilson etal., 1978). In addition, ob- study to study, a general pattern has
servations on rhesus in the outdoor envi- emerged: In most laboratories ovulatory
ronment consistently show that sexual ac- cycles and menstruation are recorded
tivity of particular females is confined to throughout most of the year, but the sum-
one or more discrete periods within the mer months typically are characterized
mating season, whereas males generally either by an increased incidence of anovu-
are observed to be sexually active through- latory cycles or a period of amenorrhea
out the months of mating (Carpenter, (Hartman, 1932; van Wagenen, 1945;
1942; Conaway and Koford, 1964; Kauf- Rowell, 1963; Keverne and Michael, 1970;
mann, 1965; Lindburg, 1971; Loy, 1971). Riesen etal., 1971).
Although there is some variability in this Thus, the distinct pattern of seasonal
pattern between geographic locations, the mating observed in the free ranging and
following general picture has emerged: compound housed rhesus is altered when
The annual onset of mating activity occurs the animals are maintained in laboratories
in late summer or early fall and continues or other controlled environments. Surveys
for a period of 4-5 mo. Similarly, births of birth records from laboratory breeding
are distributed over several months begin- colonies reveal that births occur during
ning in late winter and extending into the every month of the year, with some colo-
early summer months. Individual females nies showing an even annual distribution
are sexually active for an average duration and others some seasonal variation in
of 5-11 days, and often are sexually active monthly conception rates (Eckstein and
on multiple occasions during a single sea- Kelly, 1966; Valerio et al, 1969). A de-
son, with some of these active periods oc- tailed analysis of the pattern of concep-
curring following conception. tions and births in both free ranging and
One limitation of the data derived from laboratory colonies (Vandenbergh, 1973)
 REPRODUCTIVE BEHAVIOR IN THE RHESUS
demonstrated that the degree to which the
seasonal pattern was muted in the labora-
tory colonies may be related both to the
length of time a particular animal has been
in that environment as well as to specific
features of the environment. Vanden-
bergh (1973) also identified the photope-
riod as a possible environmental variable
which controlled the timing of the annual
mating period.
More recently, investigators have docu-
mented the characteristic pattern of ovar-
ian hormone secretion which is associated
with the menstrual cycle, and have also
demonstrated the influence of the pitu-
itary gonadotropins in regulating this cycle
(Hafez, 1974; Knobil, 1974). With respect
to sexual behavior, laboratory studies uti-
lizing the pair test paradigm consistently
demonstrate changes in the frequency of
copulations and related sexual behavior as
a function of the phase of a female's men-
strual cycle (Goy and Resko, 1972; Michael
et al, 1972; Czaja and Bielert, 1975), and
these data clearly establish that female hor-
monal variables exert an influence on non-
human primate sexual interactions. How-
ever, studies conducted in the pair cage
environment also find that copulations oc-
cur during all phases of the menstrual
cycle, albeit with lower frequency during
some phases and a clear peak at mid-cycle
(Ball and Hartman, 1935; Michael et al.,
1967; Johnson and Phoenix, 1978); this ap-
pears to differ from the pattern reported
in the field studies. Investigators have sug-
gested that the physical characteristics of
the testing environment and the social
phenomena related to repeated short term
(12 min to 1 hr) pairings may produce
changes in the copulatory pattern (Rowell,
1972; Goldfoot, 1977).
The issues
Our present knowledge of the repro-
ductive physiology and endocrinology of
the rhesus monkey has been derived from
an extensive set of experiments which have
produced an impressive understanding of
the reproductive biology of this species.
However, the precise nature of the rela-
tionship between reproductive behavior
and underlying physiological and endo-
187
crine variables is clouded by the fact that
the rhesus monkey maintained in the lab-
oratory environment differs from the rhe-
sus maintained in the outdoor environ-
ment in two significant respects: (i) the
distribution of reproductive activity on a
seasonal basis, and (ii) the distribution of
sexual activity across the menstrual cycle.
Thus, a number of questions relating to
the control and coordination of mating ac-
Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021
tivity in the rhesus monkey remain unre-
solved. Among these questions are the fol-
lowing.
(1) How does the pattern of discrete ep-
isodes of sexual receptivity in female rhe-
sus living outdoors relate to cyclic ovarian
hormone secretions?
(2) What factor or factors control the
seasonal reproductive cycle?
(3) Do environmental variables which
function to control seasonal mating pat-
terns act on males, females or both? What
mechanisms serve to ensure coordination
of mating between the sexes?
(4) How do social variables act to influ-
ence sexual activity, mating patterns, and
reproductive success?
Data obtained from social groups of rhe-
sus monkeys maintained in outdoor com-
pounds—an environment which is in some
respects a bridge between the field setting
and the laboratory setting—have provided
some additional information regarding the
coordination of reproductive phenomena
in this species.
THE DATA
Compound environment
In association with a long term research
project designed to investigate hormonal-
behavioral relationships in intact, socially
housed non-human primates, several
groups of rhesus monkeys were housed in
outdoor compounds at the Field Station of
the Yerkes Regional Primate Research
Center in Lawrenceville, Georgia, begin-
ning in September 1969. Detailed descrip-
tions of these facilities have been reported
(Gordon and Bernstein, 1973; Bernstein
and Gordon, 1977) as have statements re-
lating to husbandry and colony manage-
ment practices, routine procedures, and
188 THOMAS P. GORDON

maintenance of demographic records these studies, adult male members of a

(Bernstein and Gordon, 1977; Wilson et particular social group were placed in in-
al, 1978). Groups were maintained chiefly dividual cages, and permitted access to the
in compounds 38 m on a side, although remainder of the social group only for a
compounds of 30 m or 15 m per side were period of several hours each day. During
also used. Each of these facilities has two the male access period continuous behavior,^
features which are instrumental to the observation was maintained and a com-
methods employed: (i) an observation plat- plete record of sexual activity thus was ob-
form which provides an unrestricted view tained.
of the entire compound, and (ii) an indoor

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

area equipped with a capture partition Female sexual behavior: The fertile cycle
which provides for expeditious capture The initial experiment focused on fe-
and handling of acclimated subjects. male sexual behavior and concomitant
The research focus during the initial measures of ovarian hormones. Adult
years of the project was directed to phe- male access to the social group was restrict-
nomena other than female sexual behavior ed to 6 hr per day for a 6-wk period en-
or patterns of reproductive activity; how- compassing the typical peak of the mating
ever, it quickly became evident that social season. Blood samples were obtained twice
groups maintained in the compound en- weekly from each of 12 adult females in
vironment displayed a cycle of seasonal the group and progesterone levels were
mating similar to that observed in free determined by radioimmunoassay. These
ranging rhesus (Vandenbergh, 1973; Gor- data permitted estimation of the time of
don et al., 1976). Consequently, subse- ovulation by use of the established rela-
quent efforts have been directed toward a tionship between ovulation and a subse-
further elucidation of seasonal mating quent progesterone rise.
phenomena. Analysis of the data collected through-
out this study revealed that neither the sea-
Study methods sonal mating pattern nor the reproductive
Information relevant to the control and success rate were adversely affected by the
coordination of mating activity in com- restricted male access paradigm or the
pound housed social groups has been ob- twice weekly captures of the study group.
tained both via analysis of demographic Eleven females (92%) were impregnated
records and through the conduct of con- during the study and subsequently gave
trolled experiments. The general methods birth, a rate which is not significantly dif-
employed in the conduct of the systematic ferent from the conception and birth rates
studies, including behavioral observation typical in this colony. The median partu-
techniques, animal capture and blood sam- rition date for the 11 females was 4 May,
pling procedures, hormonal assays, and with a range from 19 March through 2
restricted access paradigms, have been de- June. These dates are similar to the par-
tailed previously (Bernstein et al., 1974; turition dates for the rhesus females in un-
Gordon etal., 1976; Cochran, 1979). disturbed groups in this colony (n = 26),
Briefly, the studies consisted of the rou- among whom the median date in the same
tine collection of both behavioral and en- year was 3 May with a range from 15
docrine data from adult male and/or fe- March through 2 July.
male monkeys maintained in social groups Behavior was observed throughout the
in outdoor compounds. The focus of the usual mating season (late September
behavioral observation was on sexual activ- through mid-December), with copulations
ity and related behaviors, while the endo- by most males recorded during all phases
crine assays measured the gonadal hor- of the study. During the restricted access
mones. Because of the limitations inherent phase, which extended from 12 October
in the use of behavioral time sampling through 21 November, a total of 255 com-
techniques, some of the experiments uti- plete copulatory series were recorded in
lized a restricted male access design. In the 216 hr of observation (1.18/hr). One
 REPRODUCTIVE BEHAVIOR IN THE RHESUS 189

or more copulations were recorded on 33

of the 36 test days (range 1-16 copula-
tions), with 8 copulations on a typical
(modal) day involving 4 males (range 1-5)
and 2 females (range 1-5).
^ T h e copulatory activity of particular fe-
males was spaced unevenly across the
study period, occurred in discrete blocks,
and snowed marked variability. Six fe-
males copulated exclusively during the 6-

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

wk restricted access phase, and the data for
these subjects were used to examine vari-
ability and the influence of social factors
on female copulatory behavior. These six
females exhibited copulatory behavior on
an average of 12 days (range 6-19 days)
and a mean of 39.6 total copulations
(range 6-74). There was not a significant
relationship between position in the social
dominance hierarchy and either total cop-
ulations (rho = .657) or total days of sex-
ual activity (rho = .542) among this subset
of six females. The range of copulations
by a particular female during a single 6 hr
session varied from 1 to 11.
The variability of copulatory behavior
and the relationship between sexual activ-
ity and assayed progesterone values is
shown in Figure 1 which depicts behavior
and progesterone concentrations for five
subjects for whom sexual behavior was lim-
ited to the restricted access phase and who
also displayed confirmation of ovulation
via rising progesterone levels during this
period. Each female abruptly terminated
all copulatory behavior concomitantly with
the sharp increase in progesterone. The
most dramatic example of this shift is pre-
sented by RWf who culminated a 10 day
period of receptivity with 10 copulations
on 17 November, then exhibited no cop-
ulations on 18 November or thereafter.
The progesterone data and recorded men-
struation clearly shows that ROf ovulated
twice within the 6 wk, with a limited series
of copulations associated with each epi-
sode. RMf displayed an abrupt termina-
tion of sexual activity as progesterone rose,
but was observed to copulate again after
an interval of 2 wk. Four additional cop-
ulations were scattered over 9 days at a
time when progesterone values dropped.
Both RIf and RHg showed the same basic
14 17 21 24 28 4 7 II 14 18 21
DATE
FIG. 1. Daily copulatory frequency and serum pro-
gesterone concentration for each of five female rhe-
sus monkeys. Data were collected 6 days/wk for 6 wk
during the mating season.
pattern although differing in the duration
and frequency of recorded copulations.
The nature of the relationship between
female copulatory behavior and ovulation
as indicated by progesterone values is
more clearly illustrated when a composite
for the five females is examined (Fig. 2).
Since all the females were impregnated,
the cycles were aligned on the rising pro-
gesterone day, with a day 4 days prior to
the first recorded rise set as day 0. Figure
2 shows the total copulations for the five
females for 10 day periods before and af-
ter this point (approximate ovulation). As
can be seen, sexual activity observed
throughout the 10 days preceding day 0,
increasing sharply in the last several days,
declines abruptly; then no behavior is ex-
hibited in the days following the proges-
terone rise. That is, in these ovulatory
cycles which resulted in fertile matings, fe-
male copulatory behavior was restricted to
the follicular phase of the cycle, peaking
at mid-cycle, and no copulatory behavior
was exhibited once the corpus luteum be-
190 THOMAS P. GORDON

TABLE 1. Complete copulatory series between males (n =

6) and those females (n = 6) whose copulatory behavior
was displayed exclusively during the 216 hr when male ac-

r
•20
cess to females was restricted to 6 hrlday.

4
16 § Female

I " _J Male RHg RAh RMf RWf RIf ROf Total©

12 RHb 15 11 15 8 11 0 60
3
a " RKa 31 20 10 2 4 1 68
g RMc 3 11 6 7 5 2 34
8 RHc 5 3 6 6 1 1 22

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

RFc 20 8 9 7 5 2 51
3 REc 0 0 0 0 0 0 0
SEX Total 74 53 46 30 26 6 235

•0
1 i—i
-10 -8 -6 -4 -2 0 «2 *4 «6 »8 • «
DAY
FIG. 2. Daily copulatory frequency and mean serum
progesterone concentration for five female rhesus
monkeys during a 20-day period marked by ovulation
and conception. Cycles were aligned on the rising
progesterone curve.
gan to secrete significant progesterone
concentrations.
Each of the females copulated with mul-
tiple males as is shown in Table 1, a matrix
of copulatory behavior observed during
the restricted access phase involving the six
females whose copulatory behavior was
limited entirely to that time. Two other
features of the distribution of copulations
provide evidence of the influence which
the hormonal status of a female had on
determining copulatory behavior in this
social context. There was a marked ten-
dency for females to mate with multiple
males on days when they were receptive,
and all of the females copulated with mul-
tiple males during the 3 days of periovu-
latory sexual activity. Secondly, there was
marked tendency for males to mate with
the same females on a given day. Thus,
although there was some apparent com-
petition among the males, their sexual
behavior on a particular day was directed
toward the female or females who were
sexually receptive.
Examination of the behavioral data,
along with the values obtained from the
progesterone assays and the subsequent
parturition dates, provides for each female
an estimate of the date of the first ovula-
tory cycle of the season (Table 2). Al-
though only 6 of the subjects were im-
pregnated during the 6-wk period when
blood samples were collected, the total pat-
tern of behavioral and endocrine data for
each of the 11 females is consistent with
the estimated date of conception obtained
by backdating 168 days from the date of
parturition. Inspection of the data sum-
marized in Table 2 demonstrates that of
the 11 females impregnated, 10 (91%) con-
ceived in association with the first period
of sexual receptivity of the mating season
and that this period of sexual activity was
linked to the initial ovulatory cycle of the
season. The exception (ROf) exhibited two
periods of sexual behavior, two clear pro-
gesterone rises and was impregnated on
the second ovulatory cycle. These data also
show that the initial ovulatory cycle of the
season among this group was distributed
across an 11-wk period extending from
early October through mid-December.
Further analysis revealed that the order in
which females ovulated was not related to
their position in the social dominance hi-
erarchy (P > .05; rho = -.030). Refer-
ence to Table 2 which lists the reproduc-
tive outcome for each female for the
preceeding birth season, does suggest one
factor which is predictive of the timing of
ovulation. Each of the first four females to
ovulate and conceive had failed to repro-
duce the previous year. Among the others,
all had surviving infants except RAh who
was nulliparous at the outset. Further-
more, the six females with surviving in-
fants gave birth in the study year within an
 REPRODUCTIVE BEHAVIOR IN THE RHESUS 191

TABLE 2. Inclusive period of observed copulations, dates of first measured progesterone rise and subsequent parturition,
estimated' date of conception, and reproductive history in the previous year for 12 sexually mature rhesus females.

Estimated Reproductive
Female Observed copulations Progesterone rise conception Parturition status prior year

1. ROc 29 Sept.-7 Oct. Prior to 14 Oct. 3 Oct. 19 Mar. Infant died

•2. RMf 15 Oct.-24 Oct. 28 Oct. 29 Oct. 14 Apr. Infant died
3. RHg 21 Oct.-9 Nov. 11 Nov. 8 Nov. 24 Apr. Stillborn
4. ROf 15 Oct.-19 Oct. 21 Oct.
9 Nov.-12 Nov. 14 Nov. 11 Nov. 27 Apr. No pregnancy
5. RIf 6 Nov.—16 Nov. 18 Nov. 26 Nov." 12 May" Infant survived
6. RWf 2 Nov.-17 Nov. 18 Nov. 18 Nov. 4 May Infant survived
7. RAh 2 Nov.-21 Nov. After 21 Nov.c 15 Nov. 1 May No pregnancy
8. RNf 19 Nov.-26 Nov. After 21 Nov.c 24 Nov. 10 May Infant survived
9. RHf 20 Nov.-4 Dec. After 21 Nov.c 4 Dec. 20 May Infant survived

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

10. RJb 10 Dec-14 Dec. After 21 Nov.c 9 Dec. 25 May Infant survived
11. RBb 15 Dec-19 Dec. After 21 Nov.c 17 Dec. 2 June Infant survived
12. RYc 11 Nov.-16 Nov. None N.A. None Infant survived
a
Date of conception estimated by backdating 168 days from date of parturition.
b
RIf gave birth on 12 May to a moribund infant which evidently was beyond term since she did not copulate
after 16 Nov.
c
Progesterone rise inferred from subsequent confirmed conception.

average of 15 days of their parturition date of the female subjects exhibited repeated
the previous year. menstrual cycles during the study which
extended from September through April,
Female sexual behavior: Repeated cycles but that only some of the menstrual cycles
The foregoing data revealed that the were associated with presumptive evidence
discrete periods of copulatory behavior ob- of ovulation (mid-cycle estrogen surge fol-
served in rhesus housed outdoors in social lowed by increased progesterone concen-
groups were correlated with hormonal trations). Copulatory behavior by females
events associated with ovulation, and was limited to ovulatory cycles. Addition-
seemed to suggest that the influence of ally, the following patterns were evident:
ovarian hormones may be greater than (i) in most subjects we detected at least one
had been demonstrated in the laboratory anovulatory cycle before the seasonal re-
environment. However, since the majority sumption of ovulation and associated sex-
of cycles examined had resulted in fertile ual activity, (ii) the first ovulatory cycle of
matings, an analysis of the effects of re- the season again occurred at varying times
peated cycles of ovarian hormones was not across a several month span, (iii) most fe-
possible. Therefore, a second study was males exhibited multiple ovulatory cycles,
conducted in which all the adult males but by April all sexual activity had termi-
were vasectomized to prevent fertile mat- nated, and no further evidence of ovula-
ings. The restricted male access paradigm tion was observed, and (iv) the predomi-
was again employed (4 hr/day) and the du- nant pattern for each female subject within
ration of the study was extended to cover a particular cycle was that copulations were
the entire annual mating season. A com- limited to the follicular phase, peaking at
plete record of copulatory behavior was mid-cycle with no copulations recorded
maintained and each female was examined during the major portion of the luteal
daily via vaginal swab to record menstrua- phase. Representative data from 11 cycles
tion. Blood samples were obtained from (7 subjects) are depicted in Figure 3, which
each female (n = 11) periodically through- graphically illustrates the typical pattern of
out the study, and radioimmunoassay was the distribution of copulations across the
employed to determine 17/8-estradiol and menstrual cycle. This general pattern was
progesterone concentrations. evident in 37 of 39 cycles which were
marked by copulatory activity and pre-
Analysis of the data revealed that each
192 THOMAS P. GORDON
FIG. 3. Daily mean copulatory frequency and mean
17/3-estradiol and mean progesterone concentrations
from 11 ovulatory cycles exhibited by seven female
rhesus monkeys. Cycles were aligned using a reverse
menstrual plot.
sumed ovulatory. In the remaining 2
cycles, both recorded in the same female
(who also exhibited three cycles of the pre-
dominant pattern) copulatory behavior
was recorded throughout the cycle. Pre-
liminary endocrine analysis suggests a pos-
sible hormonal correlate of this variant
pattern (abnormally high luteal estrogen
concentration) but this remains to be con-
firmed.
DISCUSSION AND CONCLUSIONS
The results of these experiments clearly
demonstrate that copulatory behavior in
female rhesus monkeys group living in
outdoor environments occurs in associa-
tion with ovulatory cycles and tends to be
limited to the follicular and peri-ovulatory
phases of such cycles. That is, sexual be-
havior in this species is under the precise
control of hormonal variables related to
the ovarian cycle. In this regard, the be-
havior of the rhesus monkey is similar to
the pattern observed in the vast majority
of mammalian species (Leshner, 1978) and
does not provide an example of primate
emancipation from hormonal control of
sexual behavior. The finding that rhesus
copulate throughout the menstrual cycle
in the laboratory pair test should be viewed
as a variant from the species natural pat-
tern and explanations sought in the al-
tered physical or social environment. Sim-
ilarly, the postulation that the rhesus
monkey female provides an appropriate
model for the study of human sexual be-
havior (Michael and Zumpe, 1970) mu^|
be re-evaluated.
The finding here that rhesus female
copulatory behavior varies as a function of
the ovarian cycle does not provide evi-
Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021
dence that any specific hormone or hor-
mones produce this effect. Both estrogens
(Michael and Keverne, 1968) and andro-
gens (Herbert, 1970), which also show a
peri-ovulatory peak (Hess and Resko,
1973), have been shown to influence sex-
ual activity. Since the present data are
merely correlative, our understanding of
the particular hormonal variables which
influence rhesus sexual behavior has not
been advanced. It should be noted, how-
ever, the copulatory behavior in particular
females terminated abruptly at a time
when concentrations of 17/3-estradiol and
testosterone are declining and progester-
one levels are increasing. It may be that
the confluence of several hormonal changes
produces the dramatic behavioral effect.
Previously published analyses of the
birth records from breeding populations
of rhesus monkeys demonstrated that fe-
males with surviving offspring from the
previous year conceive significantly later in
the subsequent mating season than do fe-
males who were not impregnated or who
suffered a pregnancy failure (Drickamer,
1974; Wilson etal, 1978). The observation
here that females tend to conceive during
the first ovulatory cycle of the mating sea-
son, and that the timing of the resumption
of ovulation is related to reproductive out-
come in the prior year, supports the pos-
tulation that this effect is mediated by the
antigonadal influence of prolactin which is
increased by suckling. Further evidence is
derived from the observation that suckling
in rhesus is associated with increased pro-
lactin levels and low concentrations of the
pituitary gonadotropins (Weiss et al.,
1976). Thus the presence of a surviving
infant would produce a delay in the return
to fertile ovarian cycles.
The observation that rhesus females
 REPRODUCTIVE BEHAVIOR IN THE RHESUS
housed with vasectomized males, and thus
not impregnated, ceased exhibiting ovu-
latory cycles in the spring is consistent with
Eaton's (1972) findings on the Japanese
macaque (M. fuscata), and is supportive of
gthe suggestion that day length may be the
crucial environmental determinant of the
seasonal mating pattern. The pattern of
ovarian hormone and gonadotropin secre-
tion during the non-mating season has not
been measured in the rhesus, but data
from M. fuscata, also a seasonal primate,
shows an absence of cyclic variation in
ovarian hormones during non-mating pe-
riods (Oshima etal, 1977). Although avail-
able data from primate species do not
indicate a mechanism by which day length
may influence ovulatory activity, work with
the seasonally breeding ewe (Ovis species)
suggests that a seasonal change in the feed-
back effect of 17/3-estradiol on LH secre-
tion may account for the annual pattern
(Karsch etal., 1977).
The observations made here, placed in
the context of related findings, lead to sev-
eral tentative conclusions.
(1) The seasonal mating pattern exhib-
ited by rhesus monkeys living in outdoor
environments is controlled by a variable or
variables which act on the female members
of the species to limit the occurrence of
ovulatory cycles to a certain portion of the
year.
(2) The environmental variable which
most likely plays a functional role in the
control of the seasonal mating pattern in
the rhesus monkey is the photoperiod.
Present evidence suggests that the photo-
period inhibits the occurrence of ovulatory
cycles during long days. The timing of the
seasonal resumption of ovulatory cycles in
a particular female is also influenced by
recent reproductive history, presumably
mediated by lactation and associated hor-
monal patterns.
(3) Copulatory behavior of female rhe-
sus monkeys living in social groups in out-
door environments tends to occur in dis-
crete periods typically associated with the
follicular portion of ovulatory cycles. This
pattern demonstrates that cyclic hormonal
events strongly influence sexual behavior
under these conditions. However, present
193
evidence is limited to correlational data
and a direct causal link between a partic-
ular hormone or hormones and patterns
of sexual behavior has not been demon-
strated.
(4) The altered seasonal pattern ob-
served in laboratory environments is most
likely produced by the altered physical en-
vironment. The pattern of copulations
throughout the menstrual cycle is probably
a result of social phenomena attendent to
repeated, short duration pairings—but
does demonstrate the behavioral plasticity
Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021
of the rhesus monkey.
Although some of the questions relating
to the coordination of reproductive behav-
ior in the rhesus monkey have been clari-
fied, these findings only provide a foun-
dation on which future work and
broadened understanding may be based.
ACKNOWLEDGMENTS
The research reported here has been
supported by NIMH Grant MH-20483
and by NIH Grant RR-00165. I would like
to thank Delwood C. Collins and Robert
M. Rose for the assays and to gratefully
acknowledge the assistance of Dennis Chi-
kazawa, Carol Cochran, Melissa Knauer,
Gary Mallow, Joel Volpi, and Louise
Wright.
REFERENCES
Allen, E. 1927. The menstrual cycle of the monkey,
Macacus rhesus: Observations on normal animals,
the effects of removal of the ovaries and the ef-
fects of injections of ovarian and placental ex-
tracts into the spayed animals. Contrib. Embryol.
19:1-44.
Altmann, S. A. 1962. A field study of the sociobiol-
ogy of rhesus monkeys, Macaca mulatto. Ann.
N.Y. Acad. Sci. 102:338-435.
Ball, J. and C. G. Hartman. 1935. Sexual excitability
as related to the menstrual cycle in the monkey.
Amer. J. Obstet. Gynecol. 29:117-1 19.
Bernstein, I. S. and T. P. Gordon. 1977. Behavioral
research in breeding colonies of Old World mon-
keys. Lab. Anim. Sci. 27:532-540.
Bernstein, I. S., R. M. Rose, and T. P. Gordon. 1974.
Behavioral and environmental events influenc-
ing primate testosterone levels. J. Hum. Evol.
3:517-525.
Carpenter, C. R. 1942. Sexual behavior of free rang-
ing rhesus monkeys (Macaca mulatta). 1. Speci-
mens, procedures and behavioral characteristics
of estrus. II. Periodicity of estrus, homosexual,
194 THOMAS P. GORDON

autoerotic and nonconformist behavior. J. Comp. ings of V International Congress of Endocrinology,

Psychol. 33:142-162.
Cochran, C. G. 1979. Proceptive patterns of behav-
ior throughout the menstrual cycle in female
rhesus monkeys. Behav. Neurol. Biol. 27:342-
353.
Conaway, C. H. and C. B. Koford. 1964. Estrous
cycles and mating behavior in a free-ranging
band of rhesus monkeys. J. Mammal. 45:577-
588.
Corner, G. W. 1923. Oestrus, ovulation and men-
struation. Physiol. Rev. 3:457-482.
Hamburg, July 18-24, 1976, pp. 192-198. Ex-
cerpta Medica, Amsterdam-Oxford.
Kaufmann, J. H. 1965. A three-year study of mating
behavior in a free ranging band of rhesus mon-
keys. Ecology 46:500-512.
Keverne, E. B. and R. P. Michael. 1970. Annual
changes in the menstruation of rhesus monkey!^
J. Endocrinol. 48:669-670.
Knobil, E. 1974. Maturation of the neuroendocrine
control of gonadotropin secretion in the rhesus
monkey. In M. G. Forest and J. Bertrand (eds.),

Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021

Czaja, J. A. and C. Bielert. 1975. Female rhesus sex- International symposium on sexual endocrinology of
ual behavior and distance to a male partner: Re- the perinatal period, pp. 205-218. INSERM, Paris.
lation to stage of the menstrual cycle. Arch. Sex. Leshner, A. I. 1978. An introduction to behavioral en-
Behav. 4:583-597. docrinology. Oxford University Press, N.Y.
Drickamer, L. C. 1974. Social rank, observability, Lindburg, D. G. 1971. The rhesus monkey in north
and sexual behavior of rhesus monkeys (Macaca India: An ecological and behavioral study. Prim.
mulatto). J. Reprod. Fertil. 37:117-120. Behav. 2:1-106.
Eckstein, P. and W. A. Kelly. 1966. A survey of Loy, J. 1971. Estrous behavior of free-ranging rhe-
breeding performance of rhesus monkeys in the sus monkeys (Macaca mulatto). Primates 12:1-31.
laboratory. Symp. Zool. Soc. London 17:91-112. Michael, R. P. and E. B. Keverne. 1968. Pheromones
Goldfoot, D. A. 1977. Sociosexual behaviors of non- in the communication of sexual status in pri-
human primates during development and ma- mates. Nature 218:746-749.
turity. Social and hormonal relationships. In A. Michael, R. P., E. B. Keverne, D. Zumpe, and R. W.
M. Schrier (ed.), Behavioral primatology: Advances Bonsall. 1972. Neuroendocrine factors in the
in research and theory, Vol. 1. John Wiley, New control of primate behavior. Rec. Prog. Horm.
York. Res. 28:665-706.
Gordon, T. P. and I. S. Bernstein. 1973. Seasonal Michael, R. P., G. S. Saayman, and D. Zumpe. Sexual
variation in sexual behavior of all-male rhesus attractiveness and receptivity in rhesus monkeys.
troops. Amer. J. Phys. Anthrop. 38:221-225. Nature 215:554-556.
Gordon, T. P., R. M. Rose, and I. S. Bernstein. 1976. Michael, R. P. and D. Zumpe. 1970. Rhythmic
Seasonal rhythm in plasma testosterone levels in changes in the copulatory frequency of rhesus
the rhesus monkey (Macaca mulatta): A three monkeys (Macaca mulatta) in relation to the men-
year study. Horm. Behav. 7:229-243. strual cycle and a comparison with the human
Goy, R. W. and J. A. Resko. 1972. Gonadal hor- cycle. J. Reprod. Fertil. 21:199-201.
mones and behavior of normal and pseudoher- Neville, M. K. 1968. Male leadership change in a
maphroditic nonhuman female primates. Rec. free-ranging troop of Indian rhesus monkeys
Progr. Horm. Res. 28:707-733. (Macaca mulatta). Primates 9:13-27.
Hafez, E. S. E. 1974. Comparative reproduction of non- Oshima, K., M. Hayashi, and K. Matsubayashi. 1977.
human primates. Charles C Thomas, Springfield, Progesterone levels in the Japanese monkey
Illinois. (Macaca fuscata fuscata) during the breeding and
Hartman, C. G. 1932. Studies in the reproduction nonbreeding season and pregnancy. J. Med. Pri-
of the monkey, Macacus (Pilhecus) rhesus, with matol. 6:99-107.
special reference to menstruation and pregnan- Riesen, J. W., R. K. Meyer, and R. C. Wold. 1971.
cy. Contrib. to Embryol. 134:1-161. The effect of season on the occurrence of ovu-
Herbert, J. 1970. Hormonal and reproductive be- lation in the rhesus monkey. Biol. of Reprod.
havior in rhesus and talapoin monkeys. J. Re- 5:111-114.
prod. Fertil. 11:119-140. Rowell, T. E. 1963. Behavior and female reproduc-
Hess, D. L. and J. A. Resko. 1973. The effects of tive cycles of rhesus macaques. J. Reprod. Fertil.
progesterone on the patterns of testosterone and 6:193-203.
oestradiol concentrations in the systematic plas- Rowell, T. E. 1972. Female reproductive cycles and
ma of the female rhesus monkey during the in- social behavior in primates. Adv. Stud. Behav.
ter-menstrual period. Endocrinology 92:446- 4:69-105.
453. Southwick, C. H., M. A. Beg, and M. R. Siddiqi.
Johnson, D. F. and C. H. Phoenix. 1978. Sexual be- 1961. A population survey of rhesus monkeys in
havior and hormone levels during the menstrual villages, towns, and temples of Northern India.
cycle of rhesus monkeys. Horm. Behav. 11:160- Ecology 42:698-710.
174. Valerio, D. A., A. J. Pallotta, and D. A. Courtney.
Karsch, F. J., D. L. Foster, S. J. Legan, and R. L. 1969. Experience in large scale breeding of sim-
Hauger. 1977. On the control of tonic LH se- ians for medical experimentation. Ann. N.Y.
cretion in sheep: A new concept for regulation Acad. Sci. 162:282-296.
of the estrous cycle and breeding season. In V. Vandenbergh, J. G. 1973. Environmental influences
H. T . J a m e s (ed.), Endocrinology, Vol. 1, Proceed- on breeding in rhesus monkeys. In G. H. Phoe-
 REPRODUCTIVE BEHAVIOR IN THE RHESUS
nix (ed.), Primate reproductive behavior, Vol. 2, pp.
1—19. Karger, Basel.
Vandenbergh, J. G. and S. Vessey. 1968. Seasonal
breeding of free-ranging rhesus monkeys and
related ecological factors. J. Reprod. Fertil.
15:71-79.
fean Wagenen, G. 1945. Optimal mating time for
pregnancy in the monkey. Endocrinol. 37:307-
311.
195
Weiss, G., W. R. Butler, J. Hotchkiss, D. J. Dierschke,
and E. Knobil. 1976. Periparturkional serum
concentrations of prolactin, the gonadotropins,
and the gonadal hormones in the rhesus mon-
key. Proc. Soc. Exp. Biol. Med. 151:113.
Wilson, M. E., T. P. Gordon, and I. S. Bernstein,
1978. Timing of births and reproductive success
in rhesus monkey social groups. J. Med. Prima-
tol. 7:202-212.
Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021
Downloaded from https://academic.oup.com/icb/article/21/1/185/134189 by guest on 05 March 2021