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Chimpanzee genital swelling and its role in the pattern of sociosexual behavior.

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American Journal of Primatology 28101-113 (1992)
Chimpanzee Genital Swelling and Its Role in the Pattern
of Sociosexual Behavior
Department of Obstetrics and Gynecology, University of Oklahoma College of Medicine,
Oklahoma City
Behavioral observations were made on thirteen female and seven male
adult group-living chimpanzees (Pun troglodytes). The behavioral data
were analyzed as a function of the day of the females’ menstrual cycles to
explore the possible interrelationship between genital swelling and sociosexual behavior of female chimpanzees.
Copulatory behavior was confined almost entirely to the period of genital
swelling and the occurrence of male-to-female genital inspection (both
female- and male-initiated) was negatively correlated with the days from
swelling onset, i.e., as the presumed day of ovulation approached, genital
inspection decreased, while copulatory behavior increased. In addition,
more females groomed their male cagemates during the luteal phase than
in the follicular phase of their cycles, whereas male-to-female grooming
was positively correlated with the progress of the cycle, with peaks during
the time of swelling onset and menstruation.
The profile of sociosexual behavior observed throughout the menstrual
cycle suggested that, although chimpanzees exhibit an extended period of
sexual receptivity and genital swelling, the presumed fertile period is not
concealed. The role of genital swelling in chimpanzees is discussed in
relation to the possible hormonal effect on female sexuality and the evolution of chimpanzee mating strategies. Q 1992 Wiley-Liss, Inc.
Key words: sexual behavior, sociosexual behavior, chimpanzee, Pun troglodytes, genital inspection, genital swelling
The 36 day menstrual cycle of adult female chimpanzees (Pun troglodytes) is
characterized by a cyclical change in the size, shape, and turgidity of the entire
anogenital region. There is an initial period of increasing genital swelling that
lasts an average of 7.6 days. The period of maximal swelling may last for as much
as 17 days, averaging about 10-12 days [McGinnis, 19791. The volume of interstitial fluid contained in the swelling measures almost 1.5 liters [Elder & Yerkes,
Received for publication September 10, 1991; accepted April 4, 1992.
Address reprint requests to Dr. Janette Wallis, Dept. of Obstetrics and Gynecology,University of Oklahoma College of Medicine, P.O. Box 26901, Oklahoma City, OK,73190.
1992 Wiley-Liss, Inc.
102 / Wallis
19361. A rapid decrease in the size and turgidity of the swelling occurs during the
next 4 days and the area then remains completely flat for approximately 13.6 days
[McGinnis, 19791. Menstruation occurs about midway through the phase of quiescence.
Several profiles of chimpanzee urinary [Graham et al., 1972, 1977; Lasley et
al., 1980; McArthur et al., 19811 and serum [Reyes et al., 1975; Graham, 1976;
Nadler et al., 19851 hormones have been reported [see review by Graham, 19811.
The early follicular phase shows high levels of FSH, which decrease gradually for
several days thereafter. Estrogen rises in conjunction with the occurrence of genital swelling, peaking just prior to the peak in FSH and decreasing immediately
after. A testosterone peak follows that of follicular phase estradiol [Nadler et al.,
19851. The estrogen decline, accompanied by detumescence of the genital area, is
followed by a rapid increase of progesterone that peaks in synchrony with a midluteal phase estrogen peak.
An LH peak is associated with the last day of maximal tumescence and the
resulting rapid rise in progesterone verifies that ovulation has occurred-typically
on the last one or two days of full genital swelling [Graham, 1981, 19821.
Observations of wild chimpanzees have noted the relationship between sexual
behavior and the presence of genital swelling [van Lawick-Goodall, 1968, 1969;
Nishida, 1968; Sugiyama, 1969; Tutin, 1975,19791.Studies of captive group-living
chimpanzees show the same basic pattern: copulatory frequency is highest during
genital swelling, although sexual behavior may occur in other reproductive phases
as well [Kollar et al., 1968; Lemmon & Allen, 1978; Coe et al., 1979; Tutin &
McGinnis, 1981; Wallis, 1982; Goodall, 1986; Wallis & Lemmon, 19861.
Many of the early studies of sexual activity in captive chimpanzees involved
pairing individuals for brief test periods throughout the female’s menstrual cycle.
The data indicated a copulatory increase during maximal genital swelling [Tinklepaugh, 1933; Yerkes & Elder, 1936a,b; Fish et al., 1941; Young & Orbison,
19441. A consistent finding in these studies was that the mid-luteal peak in estrogen [Fish et al., 19411not only lacked a corresponding increase in genital swelling,
but also failed to correspond with an increase in sexual behavior. It became apparent, then, that copulatory behavior is more closely correlated with the appearance of genital swelling than with high levels of estrogen, per se. Thus the inhibitory influence of progesterone during the luteal phase is similar with respect to
copulation and genital swelling.
Although the pair-test design allows the reliable recording of all sexual activity between a pair, there are certain drawbacks to studying chimpanzees in this
way, as was well recognized by the early investigators. Yerkes and Elder [1936al
noted that a multiparous female will typically present to a male with whom she is
on friendly terms during periods of maximal genital swelling. During other phases,
she will tend to ignore him or avoid his advances. If, however, the female is
recently matured or is a stranger to the male (or if the male is hostile or aggressive), Yerkes and Elder reported that mating behavior may occur a t any time of the
It is difficult to measure accurately the sexual initiative of female chimpanzees. In pair-test studies, the male may be conditioned to expect the female t o be
receptive. A male chimpanzee has the estimated capacity to ejaculate four times a
day [Short 19811; given only brief opportunities to do so, his sexual drive, particularly in the presence of an unresponsive female, may lead him to behave somewhat more aggressively than is normally observed in chimpanzees. Yerkes [19391,
therefore, predicted that when a reliable measurement of sexual initiation is assessed, the female will tend to restrict mating to the periovulatory period, whereas
Chimpanzee Genital Swelling and Behavior / 103
males-while also initiating copulations most frequently during maximal swelling-will tend to initiate outside this phase more often than females.
Yerkes [19391 also predicted that as the period of genital swelling progressed
(or as the time of ovulation approached) copulatory frequency would increase. Coe
et al. [1979] found peaks in copulatory activity, but the peak varied for individual
females. Not until field data were analyzed did it become apparent that there may,
indeed, be a change in frequency of copulation during the period of maximum
genital swelling. Tutin and McGinnis [1981] published a record of observed possessive mating for nine female chimpanzees in Gombe, compiled over several
months and calibrated into one “cycle.” They found that the highest frequency of
male possessive behavior occurred during the last three days of maximal genital
swelling. Similar findings were reported by Goodall [19861 and Takasaki [1985]
both of whom also noted that, as genital swelling increased, females mated with
adult males more than with immatures.
A detailed study of sexual activity throughout the menstrual cycle has never
been conducted on captive group-living chimpanzees. The purpose of this study was
to test Yerkes’s [1939] hypotheses that 1) the pattern of female initiation of sexual
interaction may differ from that of males when the day of the female’s reproductive
cycle is considered and 2) as the day of ovulation approaches, sexual activity will
be more likely t o occur, i.e., the presumed day of ovulation will not be hidden. Data
on sexual interactions, grooming, and genital inspection were inter-related with
the day of the cycle to examine the relationship between sociosexual behavior and
changing genital swelling levels in captive adult female chimpanzees.
At the onset of the study, the subjects were 13 sexually mature, female chimpanzees, ranging in age from nine to 22 years (mean = 14.3, SD -I 4.6).They were
members of three social groups, each containing at least one adult male. A total of
seven males, ages nine to 20 years, was present. All animals were wild-caught as
infants, captive reared, and had lived a t the Institute for Primate Studies, Norman, OK, for a t least 3 years.
The groups were housed in indoorloutdoor cages (totalling 148.8 m2) and fed
twice daily. Visual inspection of the genitalia allowed determination of genital
swelling size, recorded daily for each female. The number 1 represented no swelling; 2, partial swelling; and 3, maximal swelling. Maximal swelling was characterized by a tight, shiny appearance; when a maximally swollen female sits and/or
allows palpation of the genitalia, the skin immediately returns to full size, leaving
no indention. Although some researchers insist on using many more stages when
measuring level of female chimpanzee genital swelling, a simple system of only
three stages was chosen for this study. It is easily replicated and provides the
necessary information requested here, i.e., is swelling present? (If so, is it maximal?)
Behavioral Observations
Behavioral data were collected from May to August, 1980, and June to October, 1981. Only the behavioral observations of cycling females were included in
these analyses; all observations of pregnant and acyclic animals were omitted.
Females exhibiting the first postpartum estrous (PPE) cycle were included. The
20th day before the last day of first PPE maximal swelling was arbitrarily chosen
as the point at which observational data for those subjects were included in this
104 / Wallis
Day of Menstrual Cycle
0 2 4 6 8 1 0 1 2 1 4 1 6 1 8 2 0 2 2 2 4 2 6 2 8 1 3 2 3 4 3 6 2 4 6 8 101214161820
Days from Detumescence
.... . .-1&1&14-12-10
-8 -6 -4 -2 0 2 4 6 8 10 1214 1618..
....... .
- 8 - 6 - 4 -2 0 2 4 6 8 1 0 1 2 1 4 1 6 1 8 . . - 1 4 - 1 2 - 1 0 - 8 - 6 - 4 -2 0 2 4 6 8 10
Fig. 1. Numbering systems of the chimpanzee menstrual cycle. See text for detailed explanation.
Two or three females were observed simultaneously, if only one male was
present in a group, using a multi-focal sampling technique. Subjects were chosen
randomly and observed for an average of 30 minutes during afternoon sessions.
Only the behavioral interactions between the focal female and male cagemates
were recorded. Major behavioral categories included sexual behavior, grooming,
genital inspection, and other affiliative contact, as detailed further in Wallis and
Lemmon [19861. More than 700 hours of observation were made during data collection. However, this study includes only the 332.9 hours of data collected from
cycling females.
Method of Behavioral Analysis
The behavioral data from all female subjects were later pooled by day of the
menstrual cycle. Because of the high variability in cycle length and duration of
swelling phases, the data were analyzed twice: 1) in relation to the day of genital
swelling onset and 2) in relation to the day of detumescence (probable time of
ovulation). When the data were analyzed according to swelling (S) onset, the first
day of observable swelling was identified as day S(O), with the preceding days
numbered negatively and succeeding days numbered positively. According to average calculations, therefore, maximal swelling usually occurred around day S(4),
whereas menstruation appeared roughly ten days before swelling onset [S( - lo)].
Similarly, when the data were analyzed around the day of detumescence (D), the
last day of maximal swelling was labelled D(O), etc. Using this system, day DUO)
was the approximate day of menstrual onset. The large variability that necessitates two numbering systems must be considered when interpreting the results;
although both systems predict when menstruation is likely to occur, it is not
necessarily accurate to equate behavioral data from, for example, D(10) to that of
S(- 10). Figure 1 presents a stylized version of these two numbering systems along
with the traditional system of considering onset of menses as the start of the cycle.
For analysis and illustration, behavioral profiles were determined by calculating the percent of the sampled subjects that exhibited each behavioral category
during two day blocks of the cycle. For example, during days D(- 10) and D(-9), 11
of the 13 females were observed. Of those, five exhibited at least one femaleto-male grooming bout. Thus, the profile shows that 45% 6/11) of the sampled
females were observed to groom males on day D( - 10).
Due to violations of distributional assumptions, nonparametric tests were used
to analyze the data. By using either day S(0) or D(O) as a midpoint and by matching
the correspondingly numbered days before and after, a Wilcoxon test for correlated
samples was performed on the data to test the null hypothesis that sociosexual
behaviors would occur before and after swelling onset (or detumescence) with
identical probability. In addition, Pearson product-moment correlation coefficients
Chimpanzee Genital Swelling and Behavior / 105
were computed and tested to examine the null hypothesis that the duration of
swelling (or the approach of ovulation) had no effect on the percent of females
exhibiting each behavior. Finally, chi-square goodness-of-fit tests were used to test
the null hypothesis of uniformity in the behavioral profiles.
Behavioral Interactions Correlated With Genital Swelling
Behavioral data included analysis of 53 cycles. The average cycle length was
36.7 days. Pooling the data according to days from detumescence, genital swelling
began on about day D(-15) (mean = 15.4 days before detumescence, SD +- 4.4
days) and reached maximal size on day D(-12) (mean = 11.9, SD 5 4.4). Calculated from swelling onset, maximal genital swelling occurred on about S(4) (mean
= 3.6 days after swelling onset, SD ? 3.9 days).
Figures 2-4 illustrate the profiles of sociosexual behavior occurring throughout the subjects’ menstrual cycles, as determined by calculating the percent of
sampled females that exhibited each behavior. Median smoothing by three, as
described by Tukey [19771, was performed on some profile curves. According to
Tukey [p. 2181, “The purpose of the smooth is to show off general behavior,” thus
better illustrating the trend of the results.
Sexual behavior. Males initiated sexual interaction more often than did females. The seven males made a total of 74 copulatory attempts, with 37 (50%)
resulting in successful copulations. The 13 females solicited 40 times, and succeeded 16 (40%) times. Thereewas no significant difference in the copulatory success rates as a function of gender-initiation (x2 = .68, df = 1, ns.).
Sexual interactions were confined almost entirely to the follicular phase of the
cycle (Fig. 2a,b). A high correlation between the days of genital swelling and the
percent of subjects exhibiting both female initiated (r = 5 8 , n = 12, P<.025) and
male initiated (r= .86, n = 12, P<.005)behaviors is revealed in the follicular phase
data (Fig. 2b).
Grooming. The 13 female subjects initiated grooming of male cagemates in
a total of 77 bouts and they received grooming from 106 male-initiated bouts.
Females solicited male-to-female grooming on 27 occasions, but male’ subjects
never solicited female grooming.
The percent of females that initiated grooming bouts with males deviated
significantly from uniformity throughout the cycle (x2= 180.4, df = 22, P<.OOl, Fig.
3a). There was a larger percentage of female subjects that groomed their male
cagemates during the luteal phase than in the follicular phase (t=7.5, n = l l ,
P<.05, Fig. 3b).
Male-to-female grooming increased consistently as the cycle progressed from
day S(-22) to S( 22)(r = 567, n = 23, P<.005, Fig. 3a). However, when the data
were analyzed according to days from detumescence, male-to-female grooming
peaked during the days of swelling onset and again around time of menstruation
(Fig. 3b).
Genital inspection. The profile of male-to-female genital inspections, according to both the days from swelling onset and detumescence, are illustrated in
Figure 4. A chi-square test rejected the hypothesis of uniformity, indicating a
nonrectangular distribution (x2= 334.6, df= 22, P<.OOl). The percentage of females receiving inspection during genital swelling was higher than before swelling onset (t = 7, n = 11, P<.05).
There was a negative correlation between the incidence of genital inspections
and the days from swelling onset ( r = -.58, df=9, P<.05). Days S(20) and S(22)
106 I Wallis
Female Initiated: (Prowptivity)
H a
-22 -20 -18 -16 -14 -12 -10
-8 -6
Days from Swelling Onset
Female Initiated: (Pmceptivity)
Male Initiated: (Attnctivily)
-22 -20 -18 -16 -14 -12 -10 -8
12 14
18 20
Days from Detumescence
Fig. 2. a: Profile of total copulatory attempts and successful copulations occurring throughout the menstrual
cycle, according to swelling onset. b Profile of total copulatory attempts and successful copulations occurring
throughout the menstrual cycle, according to days from detumescence. F = follicular phase; L = luteal phase.
were excluded from this analysis because, due to their high number, they were
more likely to represent post-detumescence than swelling.
The results of this study confirm earlier reports that chimpanzee sociosexual
behavior varies across the menstrual cycle and appears to be affected by the pres-
Chimpanzee Genital Swelling and Behavior I 107
Female Initiated
- smoothed curve
Male Initiated
-22 -20 -18 -16 -14 -12 -10 -8 -6 -4
-2 0
, . .
10 12 14 16 18 20 22
Days from Swelling Onset
Female Initiated
Male Initiated
-22 -20 -18 -16 -14 -12 -10 -8 -6 -4 -2
10 12 14
16 18 20 22
Days from Detumescence
Fig. 3. a: Profile of grooming bouts occurring throughout the menstrual cycle, according to days from swelling
onset. Solid line represents median smoothing by three. See text for details. b Profile of grooming bouts
occurring throughout the menstrual cycle, according to days from detumescence.
ence of genital swelling. Social grooming was initiated by a larger percent of
females in the luteal phase than in the follicular phase, whereas males appeared
to initiate grooming more as the cycle progressed from luteal to follicular phases.
Male-to-female genital inspections occurred more when swelling was present than
108 I Wallis
Days from SwellingOnset
Days from Detumescence
Fig. 4. Profile of gential inspections occurring throughout the menstrual cycle.
when it was not and were received by more females during the first few days of
swelling. Whether increased attention to the genitalia a t swelling onset was due to
the presence of an olfactory cue or to the novelty of the visual cue is uncertain.
Sexual interactions were confined almost entirely to the follicular phase of the
cycle. Both female- and male-initiated copulatory attempts were positively correlated with the day of genital swelling. This finding supports Yerkes’s [1939] hypothesis that as ovulation approaches, sexual activity gradually increases. However, the peak in percent of subjects exhibiting these behaviors occurred slightly
before the probable day of ovulation.
Yerkes [19391 also hypothesized that female chimpanzees may tend to restrict
mating attempts to the periovulatory period, whereas males may exhibit a less
restricted pattern of attempts. Although the results of this study indicated that
males initiated copulatory bouts during phases when females did not, i.e., during
the luteal or early follicular phases (Fig. 2b), there was no overwhelming support
for this second hypothesis. Of interest is the very restricted period of male response
to female initiation; although male subjects occasionally attempted copulations
with non-swollen females, they responded to female solicitations only when the
female exhibited maximal genital swelling, on days D(-12) to D(0).
The Function of Female Chimpanzee Genital Swelling
Several authors have offered hypotheses to explain the function of genital
swelling in female primates [see discussions by Harcourt, 1981; Dixson, 1983;
Hrdy and Whitten, 19871:
1. Hrdy 119813 and Harcourt [19811 argued that genital swellings function to
Chimpanzee Genital Swelling and Behavior / 109
increase a female’s opportunity to mate with several different males, thereby increasing the amount of total male care her infant receives.
2. Clutton-Brock and Harvey 119761argued that the swelling enhances female
attractivity and generates intermale competition for access to females. This hypothesis suggests that the “best” male will win the competition and ultimately
become the father of the female’s offspring.
3. Hamilton [1984] hypothesized that genital swellings simply signal the timing of ovulation, thereby increasing paternity confidence and possible paternal
investment by one or two males.
These hypotheses are not mutually exclusive: the second hypothesis emphasizes the benefit to females, whereas the third emphasizes the benefit to males.
However, it appears that, for chimpanzees, all three hypotheses may be valid
explanations not only for the occurrence of genital swelling, but for the lengthy
duration of the swelling and the corresponding increase in sexual attractivity and
proceptivity. The following sections discuss evidence that genital swelling in chimpanzees is indeed associated with intermale competition and female choice as
suggested in the many male, best male and ovulation advertisement hypotheses.
Many-Male Hypothesis
For a female chimpanzee, there is a large number of mates from which to
choose because, unlike males, a female is not confined to a single territory. She
may copulate with any of the males in her community or she may cross into a
neighboring community and mate with any of those males [Kawanaka & Nishida,
1974; Pusey, 19791. Apparently, the only requirement for passage by females between communities is the presence of swollen genitalia; there have been no reports
of attacks on immigrant females exhibiting genital swellings [Goodall, 19861. Females thus may use their genital swelling as a “passport” to cross territorial
borders [Nishida, 1979; see Wallis, 19821.
Whether a female chooses to transfer to another community or stay within her
own, the extended phase of swelling may allow more travel time and may allow
greater opportunity for female choice by providing the ability to mate with several
males, essentially obscuring paternal assurance, and gaining paternal care from
many males.
One result of a non-investing male may be infanticide. In most cases of maleperpetrated infanticide the infanticidal male was not likely to be the father of the
infant [Suzuki, 1971; Goodall, 19771. Takahata [19851 reported infanticide of infants within the group, however, the mothers had been ranging near the territorial
border and may therefore have been associating with males of another community.
In both intergroup and intragroup encounters, therefore, male chimpanzees may
use a recent history of interaction with the female as a cue either to attack or
tolerate the infant. (In fact, this recent sexual history can occur through copulations during pregnancy [see Wallis, 1982; Wallis & Lemmon, 19861.) Thus a
lengthy duration of genital swelling may facilitate female transfer in chimpanzees
and may reduce inbreeding [Kawanaka & Nishida, 1974; Pusey, 1979,19801 and
reduce probability of infanticide [Moore, 1984; Takahata, 19851, while increasing
the number of possible mates.
The Best-Male Hypothesis
A chimpanzee male may increase his ability to monopolize a female if he leads
her to consort and copulate away from the rest of the group. Because the maintenance of a consortship requires the cooperation of the female, the male is at an
110 / Wallis
advantage if he has maintained an affiliative relationship with the female. In fact,
Tutin [19801 found that females prefer consort partners that have spent large
amounts of time with them, grooming and sharing food during non-sexual contacts.
Although there is a considerable amount of intermale competition in establishing the dominance hierarchy, there is little intracommunity aggression in
chimpanzee societies. The affiliative traits of grooming and food sharing, etc., seem
to be necessary for establishing and maintaining close male-male bonds, and the
ability to rise subsequently in the hierarchy appears to require continued use of
these behavioral characteristics [Goodall, 19861.
Nishida [19831 noted that the social skills (or social intelligence) leading to
successful alliances in agonistic relationships might have been favored by individual selection, as well as by kin selection. Because consort copulations tend to result
in conception more often that do the other mating patterns [Tutin, 19791, it appears that having affiliative traits may serve to increase male reproductive success. Therefore, in chimpanzees, intrasexual selection and intersexual selection
appear to have produced some of the same behavioral characteristics in males. If
the characteristics that make a male attractive are inherited, then a female mating with attractive males will have attractive sons who will be more likely (than
unattractive sons) to provide her with many grandchildren and, thus, increase her
inclusive fitness [see Robinson, 19821.
The lengthy duration of genital swelling in chimpanzees provides adequate
time for females to experience affiliative interactions with many males and thus
may have the effect of allowing females to exercise partner preference and choose
the “best” male [Tutin, 19801.
Ovulation Advertisement Hypothesis
It has been suggested that, due to the increased period of both receptivity and
the huge genital swelling, in addition to relatively high levels of testosterone in
females, the genus Pan may have evolved a type of “concealed ovulation” [regarding P. paniscus, see Turke, 19841. It appears, however, that although chimpanzees
exhibit an extended period of genital swelling, ovulation is not concealed. In the
present study, the results were analyzed to determine if behavior during the 10-12
day maximal swelling period occurred at a constant level or if they appeared to
vary in concert with follicular development. As noted earlier, both male- and
female-initiated copulatory attempts increased as the days of swelling progressed.
Similarly, Tutin and McGinnis [19811 found that the highest frequency of possessive behavior in wild chimpanzees occurred on the presumed day of ovulation and
the two preceding days [i.e., D(-2)-D(0)1. Furthermore, whereas the early days of
maximal swelling were marked by increased male-to-female genital inspection,
incidence of inspection declined as the swelling phase progressed (present study).
These data suggest that, although one day of maximal genital swelling may be
visually indistinguishable from the next, hormonal and olfactory changes may
affect the behavior of females and, to an even greater extent, the behavior of their
male conspecifics.
Thus, rather than concealing the occurrence of ovulation, the lengthy period of
genital swelling in chimpanzees may simply increase the time of advertising the
approach of ovulation. Chimpanzees live in very large territories and, when detumescent, females tend to spend time travelling with their mothers, siblings, and/or
own offspring; i.e., they are not typically travelling with adult males. A lengthy
period of genital swelling, therefore, is a visual indicator of sexual receptivity
Chimpanzee Genital Swelling and Behavior / 111
several days before ovulation that allows females extra time for finding, approaching, and maintaining proximity to males [Nadler, 1977; Harcourt, 19811.
1. Sexual interactions were confined almost entirely to the follicular phase of
the cycle. Furthermore, as the presumed time of ovulation approached and the
female genitalia became more tumescent, both proceptivity and attractivity increased.
2. Male-to-female genital inspections occurred most often around the time of
genital swelling onset. As the follicular phase progressed, and genitalia became
more tumescent, frequency of inspection decreased.
3. The results of this study suggest that the long period of genital swelling in
female chimpanzees does not conceal ovulation, rather it serves to advertise its
This paper was based on a study that fulfilled, in part, the requirements for a
combined doctoral degree in psychology, anthropology, and zoology from the University of Oklahoma. I wish to thank the members of my doctoral committee, Drs.
O.R. Kling, J. Lancaster, D. Mock, J. Rodgers, and P. Schwagmeyer for their
comments on earlier drafts of this manuscript. B.J. King, W.C. McGrew, R.D.
Nadler and D.A. Collins offered additional advice.
Finally, I thank the late Dr. William Burton Lemmon, who first encouraged
me to pursue a career in primatology and who offered advice, guidance and, most
importantly, unrestricted access to the study subjects. This paper is dedicated to
his memory.
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genital, behavior, patterns, chimpanzee, role, swelling, sociosexual
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