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This is to certify that the

dissertation entitled

Sexual Maturation of Female
Saguinus oedipus oedlgus

presented by

Suzette Davis Tardif

has been accepted towards fulfillment
of the requirements for

Ph. D . degree in Zoology

 

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Date June 22, 1982

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SEXUAL MATURATION OF FEMALE SAQUINU§ OEDIPU§ OEDIPUS

by

Suzette Davis Tardif

A DISSERTATION

Submitted to
Michigan State University
in partial fulfilhment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Zoology

1982

ABSTRACT

SEXUAL HATURATION or FEMALE sgcumus QEQIPU§ m

by

Suzette Davis Tardif

The first hypothesis tested was that gaggiggg.gggipg§‘ggdipgg

females housed with adult males would mature, sexually, at an earlier
age than females remaining in their natal groups. The second
hypothesis was that certain behavioral interactions involving young
females would change in frequency when the females matured.

Seven females were housed with strange unrelated males. Five
females remained in their natal groups. Blood samples were taken
twice weekly and the plasma was assayed for progesterone.‘ Sexual
maturation.was defined as that age at which plasma progesterone levels
became consistently detectable. Females housed with males did mature
at an earlier age than females remaining in their natal groups.

Groups were observed for an average of three, 20-minute periods,
each week, during which time the frequency of selected interactions
was recorded. It was hypothesized that sexual and affiliative
interactions in young female-adult male pairs would increase when the
females matured. The frequency of these interactions did not increase
with maturation.

It was hypothesized that affiliative interactions between mothers
and daughters would decrease while agonistic interactions between them
would increase when the daughters matured. The mothers interactions

with their daughters were unchanged by the daughters’ maturation. No

conclusion could be drawn concerning changes in the daughters’
affiliative behavior. Aggression by daughters toward their mothers
was infrequent and did not change with the daughters’ maturation. The
variation between daughters was partially accounted for by the fact
that some natal groups contained unrelated males.

It was hypothesized that all females would mark.more when mature.
Females with unrelated males, either alone or as part of their natal
group, displayed an.increase inumarking. However, mature females in
natal groups, alone, showed no increase.

In summary, social environment did affect maturation age. The
mother’s presence was not related to the daughter’s maturation age.
However, whether the natal group, as a whole, inhibited maturation, or
unrelated males accelerated maturation, or both, remains unknown.

Most of the behavioral interactions involving maturing females were
unchanged by maturation. There was some indication that certain
behaviors were affected by maturation, but only if a strange unrelated

male was present.

ACKNOWLEDGEMENTS

I thank Dr. John A. King for his guidance and assistance
throughout my graduate education. The time and efforts of the other
members of my graduate committee at Michigan State University, Drs. W.
Richard Dukelow and Lynwood Clemens, are gratefully acknowledged. I
thank Dr. Gisela Epple for her assistance as an outside member of my
committee. Also, the assistance and tremendous moral support of Dr.
Gayle Littlefield is most gratefully acknowledged.

Financial support was provided through the Divisions of University
Programs and Medical and Health Sciences,.0ak Ridge Associated
Universities. My thanks go to Dr. C.C. Lushbaugh for providing
support which made completion of this project possible. Others at
O.R.A.U. whose efforts should be acknowledged are members of the
animal caretaker staff.

I thank Richard Tardif for providing technical and moral support
which was also necessary for completion of this project.

Finally, my special thanks go to Dr. Conrad B. Richter. His
enthusiasm for callitrichid research and his efforts in this area
provided the incentive and continued support which made this project

possible.

ii

TABLE OF CONTENTS

Page
LIST OF TABLEI I I I I I I I I I I I I I I I I I I I I I I I I I iv

LIST OF Flam I I I I I I I I I I I I I I I I I I I I I I I I I I v
mmonUCTION I I I I I I I I I I I I I I I I I I I I I I I I I I I I 1
m 1 LIWM EVER I I I I I I I I I I I I I I I I‘ I I I I 7
IntIOduCtiono I I I I I I I I I I I I I I I I I I I I I I I I I 7
Sexual Maturation-Endocrine Events. . . . . . . . . . . . . . . 9
Measuring Sexual Maturation. . . . . . . . . . . . . . . . . . 12
Sexual Maturation-Behavioral Events. . . . . . . . . . . . . . 15

Social Influences on Sexual Maturation. . . . . . . . . . . . 21

CHAPTER 2 COMPARISON OF MATURATION AGE OF FEMALES
WITH MALES AND FEMALES IN NATAL GROUPS. . . . . . . . . 26

athOdsI I I I I I I I I I I I I I I I I I I I I I I I I I I I 26
Result‘I I I I I I I I I I I I I I I I I I I I I I I I I I I I 34
Discussion and Conclusions. . . . . . . . . . . . . . . . . . 47
CHAPTER 3 BEHAVIORAL CHANGES ASSOCIATED VITH SEXUAL MATURATION. . 51
kthOdSI I I I I I I I I I I I I I I I I I I I I I I I I I I I 52
Results. I I I I I I I I I I I I I I I I I I I I I I I I I I I 55
Discussion and Conclusions. . . . . . . . . . . . . . . . . . 70

6mm DISCUSS ION I I I I I I I I I I I I I I I I I I I I I I I I 7 5

BIBLIOGMPBY I I I I I I I I I I I I I I I I I I I I I I I I I I I 84

iii

LIST OF TABLES

Table Page
1. A description of the social groupings in which the

subjects were housed. Infant < 5 months; Juvenile

> 5 months but < 24 months; Adult > 24 months.. . . . . . . . 27
2I AIIIy valid‘tionI I I I I I I I I I I I I I I I I I I I I I I 33

3. Number of females mature at 550 days. . . . . . . . . . . . . 46

4. Number of observation periods. . . . . . . . . . . . . . . . 56

iv

LIST OF FIGURES

Figure Page
1. Ages through which each female was examined. . . . . . . . . 28
2. Plasma progesterone levels of females housed with males. . . 35
3. Plasma progesterone levels of females in natal groups. . . . 41
4. Male-initiated contact frequencies. . . . . . . . . . . . . 57
5. Female-initiated contact frequencies. . . . . . . . . . . . 58
6. Female marking frequencies. . . . . . . . . . . . . . . . . 61
7. Mother-initiated contact frequencies. . . . . . . . . . . . 62
8. Daughter-initiated contact frequencies. . . . . . . . . . . 62
9. Percent of periods in which grooming occurred. . . i . . . 63
10. Percent of periods in which cuffing occurred. . . . . . . 65
11. Percent of periods in which the daughter grimaced. . . . . 66
12. Mother (left) and daughter (right) marking frequencies. . . 68

13. Marking frequencies of immature daughters. . . . . . . . . 69

INTRODUCTION

One of the pivotal events in the development of a female mammal is
sexual maturation. Sexual maturation constitutes numerous changes in
a female’s physiology, morphology and behavior. Her reproductive
system is altered from a state of quiescence to one in which
follicular maturation and ovulation occur in a regular, cyclical
fashion. The endocrine changes which cause and result from this
change in ovarian function also bring about various morphological
changes such as vaginal introitus in rodents (Donovan and Van der
Nerff ten Bosch, 1959; Rogers and Beuchmmp, 1974) and perineal
swelling in many primates (Howell, 1977; Wolfe, 1978). In addition to
morphological changes, various behavioral changes may also accompany
sexual maturation. In some rodent species, the occurrence of certain
behaviors, such as lordosis, is very clearly linked to ovarian hormone
levels common to a sexually mature, estrous female (Leshner, 1978).
However, most behavioral changes associated with sexual maturation in
most species are not so clearly linked to specific hormonal changes.
The behavioral changes that a female will display at sexual maturation
obviously depend upon a number of factors, such as her prior
experience and the age, sex, and prior experience of others in her
social group.

The age at which a female will begin sexual maturation can be

affected by a number of factors. Weight (Nilen and Naftolin, 1977).

2
nutrition (Zachiarias and Wurtman, 1969), and stress (Christian, 1978)
are known to affect maturation rate. The social environment of a
young female may also affect her maturation rate. This effect is most
amply illustrated in rodents, where the presence of a male, or male
urine, may speed up sexual maturation in young females (Kennedy and
Brown, 1970; Vandenbergh, 1967, 1969). It has also been found that,
in some cases, adult females may inhibit sexual maturation in young
females (Cowley and Wise, 1972; Drickamer, 1982; Payman and Swanson,
1980; Rogers and Beauchamp, 1976). There is also some anecdotal
evidence indicating that, in certain monogamous mammals, mothers may
inhibit sexual maturation in their daughters, through some unknown
mechanisms (Kleiman, in press; Seal, 3; 51,, 1979).

This study is an examination of the process of female sexual
maturation in the cotton-top tamarin, Sgggipug.ggdipgg,gggipgg, a
South-American primate of the family, Callitrichidae. Two types of
questions are addressed. The first question is whether the type of
social grouping in which a young female lives affects the rate of her
sexual maturation. Specifically, is there a difference between the
maturation rate of a female housed with a strange adult male and a
female housed with her natal group (i.e., her parents and various
siblings)? Second, the effect of sexual maturation on various social
interactions is examined. Specifically are male-female interactions
in mated pairs and mother-daughter interactions in natal groups
changed by the sexual maturation of the young females?

In captivity, callitrichids are generally housed as nuclear
families, that is, as one mated pair with a number of their sets of

twin offspring. Generally, the mother is the only female in the group

3
who reproduces, regardless of the number of adult female offspring
present (Epple, 1967,1970a,1975a; Kleiman, in press; Rothe, 1975).
This pattern is similar to that seen in other monogamous mammalian
species, such as the wolf, the dwarf mongoose, and the gibbon and
siamang (Kleiman, 1977; Mech, 1970; Rasa, 1972, 1973; Seal, gtflglg,
1979; Zimen, 1975). .

The means by which reproduction is limited to the mother in
callitrichid groups is not clear but it is hypothesized that the
mother suppresses the sexual maturation of her daughters (Kleiman, in
press). Generally, the reproductive state of the daughters in
callitrichid groups is unknown, as callitrichid females do not display
any reliable external signs of estrus or maturation (Hearn, g5.gl,,
1975). Assays of ovarian hormones in blood or urine of daughters in
two callitrichid species yield conflicting results. Rats and Epple
(1979) report that ovarian hormonal cyclicity is suppressed in young
Saguinga fgsciggllis females up to two years of age, if they remain in
their natal groups. However, Abbott and Hearn (personal
communication) each report that young Callithrix jacchus females who
are housed in their natal groups do cycle.

Results from studies of various species having a monogamous social
structure similar to that of callitrichids indicate that females do
mature while with their parents, but at a significantly later age than
young in closely related taxonomic groups without a monogamous social
structure. For example, female wolves generally mature at around two
years of age, compared to ten months for the closely related
domesticated dog (Seal, gt,§;‘, 1979). Similarly, beaver and dwarf

mongoose mature significantly later than closely related species

(Kleiman, 1977).

Whether the presence of a strange adult male has an effect on
the maturation rate of callitrichid females is unclear. Epple and
Katz (1980) and Abbott and Hearn (1978) report earlier ages of first
conception in females housed with adult males versus females housed
with same-aged males. However, no data are presented on the age of
sexual maturation of these females. As stated previously, the
faciliatory effect of adult males on female sexual maturation has been
amply illustrated in rodents. Based upon the information available on
the maturation rate of young females in monogamous family groups, the
effect of an adult male upon conception age in callitrichids and the
general faciliatory effect of adult males demonstrated in other
species, it is hypothesized that young females housed with males will
mature significantly earlier than females housed with their natal
groups. J

Various types of social interactions might be expected to change
when a young female begins sexual maturation. Among these, one might
expect changes in.male-female and mother-daughter interactions.

First, probable changes in male-female interactions will be addressed,
then those changes likely in mother-daughter relations.

One might reasonably suggest that sexual behavior is likely to be
affected by sexual maturation. In many primate species, including
some callitrichids, sexual behaviors are displayed by immature
individuals, though frequently in an incomplete form (Goldfoot, 1977).
Therefore, sexual maturation does not appear to be necessary for the
display of sexual behavior. However, in some primates, the frequency

of occurrence of certain sexual behavior appears to change as the

5
female matures (Hanby and Brown, 1974; Wolfe, 1978). It is
hypothesized that, in young female-adult male pairs, sexual activity
will increase when the female begins sexual maturation.

In monogamous mammals, affiliative behaviors, such as contact and
grooming, appear to serve an important role in establishing and
maintaining the pair bond. In some monogamous species, sexual
activity is reported to be relatively infrequent while affiliative
behavior are frequently displayed (Kleiman, 1977; Epple and Katz,
1980). It seems reasonable to assume that this bonding between mates
would be dependent upon the sexual maturity of both partners. For
this reason, it is hypothesized that affiliative interactions in young
female-adult male pairs will increase when the female begins sexual
maturation.

There are many questions concerning the relationship between
callitrichid mothers and daughters which remain unanswered. As
mentioned previously, it has been hypothesized that mothers suppress
the sexual maturation of their daughters through some unidentified
mechanisms. However, the evidence relative to this hypothesis is
conflicting. Similarly, reports of the interactions of adult
daughters and their mothers indicate a wide variety of responses.
Rothe (1975) reports that, in Cgllithrix ' cchus, daughters are left
with their parents for over four years with no increases in agonistic
interactions. Rothe (1978) also finds that older daughters tend to
have the fewest social contacts with both parents. Other reports on
various callitrichids indicate that agonistic interactions between
mother and daughter increase as the daughter grows older, frequently

becoming quite severe, at ages even younger than four years (Lorenz,

6
1972; Mallinson, 1975; Snyder, 1972).

Any relationship between these increases in aggression and changes
in the daughter’s maturation state are unknown, since the daughter’s
maturation state is generally unknown. However, a link between
increases in agonistic interactions between mother and daughter and
the daughter’s sexual maturation is documented in another monogamous
mammal, the wolf (Zimen, 1975), and is suggested in other species,
such as the dwarf mongoose (Rasa, 1972,1973) and the siamang (Fox,
1972). Therefore, it is hypothesized that in §‘_gggipug, a species
which also appears to be monogamous, affiliative interactions between
mother and daughter will decrease and agonistic interactions will
increase when the daughter begins sexual maturation.

Another behavior which might be expected to be affected by sexual
maturation is marking frequency. Callitrichids possess highly
developed scent glands and marking is a frequent activity of both
sexes (Epple, 1967). A number of functions have been attributed to
callitrichid scent marking, including sexual signalling (Epple, 1967;
French and Snowdon, in press), delineation of territory (Epple,
1967,1970b; French and Snowdon, in press), and expression of
frustration or excitement (Epple, 1967; Kleiman and Mack, 1980).
Because marking is associated with at least the first two of these
functions, its frequency might be expected to vary according to
reproductive state. It is then hypothesized that all females will

display an increase in marking when they begin sexual maturation.

CHAPTER 1

LITERATURE REVIEW

In uc ' n

The cottonrtop, or created bare-faced.tamarin,lgaguipug‘ggdipug
gggipgg, is a small, squirrel-like primate inhabiting the tropical
forests of northwestern Colombia (Hershkovitz, 1977). figgggggipgg is
a member of the family, Callitrichidae. Callitrichids are
characterized by small size (100-600 grams), presence of claws on all
digits except the hallux, which bears a nail, highly developed sensory
vibrissae, highly developed apocrine and holocrine sebaceous scent
glands, and generally primitive skeletal features. They are diurnal
and omnivorous (Hershkovitz, 1977).

There have been only two general field studies of,§, gggipus
(Dawson, 1978, §.g. m; Neyman, 1978, §.g. ggdipus), but these,
combined with field studies on related species (Izawa, 1978; Moynihan,
1970; Stevenson, 1978; Thorington, 1968) and numerous studies on
various captive callitrichids (Box, 1975; Epple, 1967, 1970, 1975a,
1975b, 1978; Hoage, 1978, in press; Ingram, 1977; Kleiman, 1979;
Kleiman and Mack, 1980; Rothe, 1978; Snyder, 1972; Stevenson and
Poole, 1976; Vogt, 1978a, 1978b; Welker and Luhrman, 1978; Wolters,
1978), provide some information on the probable social organization of
this species. In captivity, callitrichids are generally housed as

nuclear families, that is, as one mated pair with a number of their

8

sets of twin offspring (Epple, 1970s, 1975s; Fitzgerald, 1935;
Hiddleston, 1976; Kleiman, in press; Lorenz, 1972; Mallinson, 1975;
Rothe, 1975; Snyder, 1972). Attempts have been made to maintain
groups with more than one unrelated member of the same sex, but these
groups have almost always proven to be unstable, due to fighting
between members of the same sex. The aggression is usually most
extreme between adult females (Abbott and Hearn, 1978; Epple, 1967;
Hampton,.gtlg;,, 1966; Hiddleston, 1976; Lorenz, 1972; Rothe, 1975).

In general, only one female in a captive callitrichid group
reproduces regardless of the number of adult females present (Abbott
and Hearn, 1978; Epple, 1967, 1970a, 1975a; Hampton, gt‘glg, 1966;
Kleiman, in press; Rothe, 1975). Field studies indicate that there is
probably also only one reproducing female in wild groups (Dawson,
1978; Neyman, 1977; Stevenson, 1978). Callitrichids generally produce
fraternal twins, rarely singletons or triplets (Hershkovitz, 1977).
All family members participate in the care of the offspring, which
includes continuously carrying them from one to five weeks of age
(Epple, 1975b; Hoage, 1978; Ingram, 1977) and either sharing food or
allowing them to take food from hand (Epple, 1967; Brown and Mack,
1978). The relative contributions to infant care by the mother,
father, and older siblings apparentally vary according to species,
age, and social experience (Box, 1975; Brown and Mack, 1978; Epple,
1975b; Hoage, 1978; Ingram, 1977; Vogt, 1978a, 1978b).

The means by which reproduction is limited to only the mother in
the family group is not clear. Young females may be physiologically
inhibited. Katz and Epple (1979) report that ovarian hormonal

cyclicity is suppressed in young Saguinus fuscicgllis females within

9
their family group. However, J.P. Hearn and D.H. Abbott (personal
communication) report that young ggllithri§.jag§hgg females housed in
their family groups do cycle. Also unclear is whether limitation of
reproduction to the nether may be the result of behavioral suppression
of daughters through agonistic interactions. Parents remain quite
tolerant of their offspring, generally, up to around two years of age.
Parents are reported to be tolerant of offspring in some groups, while
quite aggressive in others, once the offspring are older than two to
three years (Kleiman, 1979; Mallinson, 1975; Rothe, 1975; Snyder,
1972). Parent-offspring aggression is also reported in the closely
related Cgllimigo (Lorenz, 1972).

The research which will be presented here is an attempt to
discover whether the reproductive potential of young female
callitrichids is controlled by social influences and how their
reproductive state, in turn, affects their social interactions. The
literature reviewed deals with the delineation of endocrine and
behavioral changes associated with puberty in female mammals,
primarily among species which exhibit a monogamous family social
structure. The influence of social interactions on maturation will

also be addressed.

Sexual Maturatign-Endgcging Events

In a post-pubescent female mammal, an endocrine feedback system
involving the ovaries, pituitary and hypothalamus controls the events
surrounding ovulation and physiological preparation for pregnancy. The
general description of these processes, presented here, will be drawn

from the literature on rodent and primate reproduction. While the

10
extensive studies of the reproduction of domesticated animals have
been reviewed (Feder, 1981; Legan and Rarsch, 1979; Odell, gtmg;,,
1970). they will not be considered here.

Gonadotropin releasing hormone (GRH) from the hypothalamus
reaches the pituitary via the hypophyseal portal system
(Turgeon,1980). The regular, pulsatile release of GRH results in the
secretion of follicle-stimluating hormone (FSH) and luteinizing
hormone (LH) by the pituitary (Knobil, 1980; Knobil, 5;.glg, 1980).
FSH acts upon the ovary, resulting in the maturation of follicles
(Richards, 1980; Turner and Bagnara, 1971). The maturing follicles
produce estrogens, probably through the combined activity of the theca
and granulosa cells (Richards, 1980). Increasing estrogen levels act
as a negative feedback to the pituitary, resulting in a relatively
steady output of FSH and LH (Dierschke, ggflglg, 1974a; Knobil, 1980;
Turner and Bagnara, 1971). There is also some evidence that FSH can
be independently controlled by factors produced by the dominnant
follicle (e.g. inhibin) (Dukelow, personal communication). However,
when estrogen reaches a certain critical level and remains at that
level for a sufficient time, the estrogen acts as a positive feedback,
causing a surge of LH (Turner and Bagnara, 1971) and FSH (Dierschke,
gt‘glg, 1973) to be released. This gonadotropin surge may be due to
increased GRH release from the hypothalamus (Fink, 1979; Turgeon,
1980). It has also been hypothesized that the surge is a result of
direct estrogen action on the pituitary (Rnobi1,,ggiglg, 1980). These
different mechanisms may reflect a taxonomic difference (Fink, 1979;
Knobil, 35.51,, 1980). The surge results in the ovulation of a mature

follicle. With ovulation, a corpus luteum is formed in the ovary from

11
the remaining theca (Mossman and Duke, 1973). Estrogen levels decline
and progesterone, produced by the corpus luteum, induces changes in
the endometrium in preparation for pregnancy (Turner and Bagnara,
1971; Mossman and Duke, 1973). Increasing levels of progesterone also
inhibit LH and FSH release (Dierschke, gt.gl,, 1973). If
fertilization and implantation do not occur, the corpus luteum
regresses resulting in a decrease in progesterone levels.

The process of puberty alters a female from a state in which
follicular maturation is not completed and ovulation does not occur to
one in which follicular maturation and ovulation occur in a regular,
cyclical, fashion. Puberty is a long, complex process involving
changes in hypothalamic, pituitary, and ovarian function. At present,
there are two hypotheses regarding the pivotal events in the
initiation of puberty. One theory contends that, prior to puberty,
the estrogen levels required to inhibit gonadotropin secretion are
quite low (Donovan and Van der Werff ten Bosch, 1959; Grumbach, 1975;
Van der Werff ten Bosch, 1975). With low levels of FSH and LH, due to
the low setting of the hypothalamic-pituitary "gonadostat", follicular
maturation does not proceed. At puberty, this gonadostat gradually
becomes re-set at a higher level, so that much higher levels of
estrogens are required to inhibit gonadotropin release. At this
stage, FSH and LH levels rise and follicular maturation begins
(Grumbach, 1975; Van der Werff ten Bosch, 1975). The second theory
contends that low gonadotrOpin levels in pre-pubescent females are not
due to a highly sensitive negative feedback system. This view is
supported by the fact that ovariectomy in pre-pubscent female Magggg

does not result in immediate gonadotropin increases as it does in

12
adult females (Dierschke,.g§,§;,, 1974a). According to this view,
changes in the hypothalamus, and possibly other areas of the CNS,
which result in a regular, pulsatile release of GRH to the pituitary
'are the pivotal events in the initiation of maturation. An
experimental demonstration of this view is seen in the fact that
pre-pubescent female,flgggg§_may be induced to mature, simply by
exogenous, regular administration of GRH (Wildt,.§§‘gl,, 1980). These
different mechanisms may, again, express taxonomic differences
(Dierschke, 3;,alg, 1974a). The negative feedback system appears to
become effective some time before the positive feedback effects of
estrogen are established (Dierschke, gt_§l‘, 1974a). Therefore, the
pubescent female will frequently not ovulate. When the positive
feedback effect of high estrogen levels is established, the female
will then ovulate and experience the complete estrous cycle, including
corpus luteum formation and subsequent rises in progesterone levels

(Richards, 1980).

mmmuain

Clearly, puberty in a female mammal is an extended and complex
process which initiates various changes in the female’s physiology,
morphology and behavior. Measurement of these various changes will
provide different levels of information about the female’s stage of
maturation.

Examination of the ovary, through histology (Dierschke, gtflglg,
1974a; Feder, 1981; Mossman and Duke, 1973) or laparoscopy (Dukelow,
gt,gl‘, 1971; Dukelow, 1975) may reveal ovulation sites or corpora

lutea. Examination of the ovary, then provides direct evidence of

13
ovarian function.

Measurement of the levels of pituitary and ovarian hormones, or
their metabolites, in blood or urine may also provide information
concerning state of maturation. The use of such endocrine measures
has become increasingly common with the development of extremely
sensitive assay methods, such as radioimmunoassay (Abraham, gtflglg,
1971; Butcher, gt_a;‘, 1974; Monroe, gtflalg, 1970; Yalow and Berson,
1971; Yamaji, gtflglg, 1973) and competitive protein binding assay
(Butcher,‘g§‘;;,, 1974; Preslock,‘gt.g;,, 1973). Increases in LH, FSH
and estrogen levels are interpreted as indicating the initiation of
puberty, when the hypothalamic-pituitary-gonadal negative feedback
system is beginning to operate as it does in a mature female
(Dierschke, g;.g;,, 1974b; Grumbach, 1974). A surge in the LH level
and a subsequent rise in progesterone level are interpreted as
indicating the completed maturation of the positive feedback system,
with ovulation and subsequent corpus luteum formation (Abbott, 1978a,
1978b; Abbott and Hearn, 1978; Dierschke, g§,a;,, 1974b; Grumbach,
1974) .

The changes in ovarian hormone levels which are initiated at
puberty result in a wide variety of morphological changes. One effect
of fluctuating estrogen levels is cyclical changes in the exfoliated
cells of the vagina. An increasing estrogen level, such as that
occurring during the follicular phase of the estrous cycle, results in
growth and cornification of the vaginal epithelium, which can be
observed and quantified with properly stained vaginal smears (Naib,
1970; Turner and Bagnara, 1971). Vaginal smears have been used

successfully to determine estrous cycle stage (Turner and Bagnara,

14
1971) and to document sexual maturation (Ramirez and Sawyer, 1965) in
rodents, but results of vaginal smears in primates have been highly
variable (Hearn and Lunn, 1975; Lang, 1967; Rosenblum and Cooper,
1968; Wan and Balin, 1969).

The development of a variety of morphological characteristics in
female mammals may be initiated by the rises in ovarian steroid levels
that begin at puberty (Goldman, 1981). These characteristics are
frequently used as indicators of sexual maturation. In rodents,
vaginal introitus and pelage changes are sometimes used as indicators
of puberty (Rogers and Beauchamp, 1974). Mature females of many
primate species exhibit swelling and color changes of the perineal
skin at estrus (Alvarez, 1973; Rowell, 1970) and the onset of these
swellings, combined with onset of menstruation, is used as an
indicator of a female’s first estrus‘(Rowell, 1977; Wolfe, 1978).
While most studies in.which perineal swelling has been used as an
indicator of reproductive state have been conducted on Old World
primates, at least one New World primate, the bowler monkey (512255;).
also exhibits cyclical perineal swelling (Glander, 1980).

The relationship of these morphological, histological and hormonal
measurements to the age at which a female is actually able to
reproduce is variable. In any mammalian species, changes which are
indicative of rising estrogen titers, only, may indicate that a female
had entered puberty but is not ovulating and is still unable to
reproduce. The length of time between the point at which a female
enters puberty and that at which she is regularly ovulating is
variable, both within and between species (Dierschke, gt,§l,, 1974b;

Rowell, 1977).

15

Certain measures indicate that a female is ovulating, e.g. those
indicating cyclical rises in progesterone levels. However, young
ovulating females frequently have insufficient luteal phases and would
be incapable of successfully reproducing (Vihko and Apter, 1981).
There may also be various behavioral inhibitions to reproduction.
These are discussed in a later section.

As a final measure of sexual maturation, age at first parturition
or first conception is sometimes used (Drickamer, 1974; Epple and

Katz, 1980; Wilson and Gordon, 1980).

Sggggl ygturation-thaviogal Events

Along with the various physiological and morphological changes
already described, the pubescent female mammal may also experience
behavioral changes. The specific behavioral changes that a given
female will display obviously vary across different taxonomic groups.
The changes will also vary within a species, according to a female’s
prior experience and the sex, age, and experience of others in her
social group. As described previously, callitrichids appear to have a
monogamous family social structure. Therefore, this review of the
behavioral effects of female sexual maturation will concentrate on
some of those interactions which a young female might be expected to
experience within a species displaying such a social structure:
interactions with a mate and interactions with parents.

‘Lgtgrggtiggg‘gigh‘g‘gggg, Sexual interactions might reasonably be
expected to be affected by the hormonal changes of puberty. The most
extensive evidence concerning the effect of ovarian steriods on sexual

behavior involve the study of adult sexual behavior. Most female

16
mammals that have been studied display some qualitative or
quantitative cyclicity of sexual behavior, relative to the estrous
cycle (Feder, 1981; Leshner, 1978; Luttge, 1971; Nadler, 1975; Rowell,
1972; Scruton and Herbert, 1970). In general, primates display a much
less distinct behavioral estrus than other mammals (Leshner, 1978) but
there is much variability within primates (Michael and Welegalla,
1968; Nadler, 1975; Rowell, 1972). Within callitrichids, Hearn and
Lunn (1975) report no quantitative or qualitative changes in sexual
behavior throughout the estrous cycle in lelighrix jgcchus while
Kleiman (1978) reports cyclicity in the frequency of sexual behavior
in ngntgpithecug rosalig.

In addition to realizing the correlation between estrous cycle
stage and occurrence of sexual behavior, may workers have discovered
effects of ovarian steroid manipulations on sexual behavior.
Generally, the removal of estrogens, usually through ovariectomy,
reduces or eliminates female sexual behavior while the administration
of exogenous estrogen re-establishes sexual behavior (Arai and Gorski,
1968; Ball, 1936; Davidson,‘g§.§;,, 1968; Dixson, £5 21,, 1973;
Goldfoot, 1977; Luttge, 1971; Luttge, gt,al,, 1975). Again, it has
been demonstrated that sexual behavior is less affected by hormonal
state in primates than in most other mammals. In some rodent species,
the administration of progesterone may facilitate or inhibit sexual
response, depending upon the relationship between progesterone and
estrogen administration (Powers, 1970; Wallen, gt‘gl., 1975).

However, in primates, progesterone administration appears to have a
general inhibitory effect on sexual response (Michael, 1968; Michael

and Zumpe, 1970).

17

The evidence, then, points to a relationship between the levels of
ovarian steroids and female sexual response. Unfortunately, there is
very little available in the way of direct evidence of the relationsip
between changes in ovarian steroids at puberty and sexual response.

In many primate species, adult sexual behaviors, such as presenting
and mounting, are displayed by infants and juveniles, though
frequently in an incomplete form (Goldfoot, 1977). Therefore, an
adult hormonal state does not appear to be necessary for the display
of some sexual behaviors. However, the frequency of occurrence of
certain sexual behaviors, as well as the fonm in which they occur,
appear to change as the female matures. In studies of macaques, it
has been found that young females become both more sexually responsive
and more attractive to males as they mature (Hanby and Brown, 1974;
.Wolfe, 1978). Obviously as a female grows older, many factors may
contribute to changes in behavior. As the changes in hormonal state
of the females in the studies cited above were neither directly
assayed or manipulated, the results do not actually provide direct
evidence of a link between the hormonal changes of puberty and sexual
response.

.Igtgggggigggwgith gaggnts, In captivity, callitrichids are most
successfully housed and reared in a family social structure. This
social structure is similar to that which is known to occur naturally
in a number of diverse mammalian species, such as wolves, as well as
some other canids, beavers, certain mongoose species, gibbons, and
siamangs (Kleiman, 1977). This review of the relationship of female
maturation to interactions with family members will be taken from the

literature on callitrichids and those species with similar social

18
structure.

Females in.monogamous species generally mature at a later age than
polygamous females in closely related species (Kleiman, 1977). Up to
the age of sexual maturation, relations between young females and
parents are generally close and harmonious. When females begin to
mature sexually a variety of changes are reported to occur in the
various monogamous species, but they all tend to be changes leading to
increased aggression toward or exclusion of the young female. In
wolves and mongooses, daughters may remain in a social group with
'their parents well past the age of sexual maturation, but their
interactions with one or both parents will be more agonistic, with the
parent(s) dominating the daughter. These agonistic interactions will
be particularly prevalent during the breeding season (Fox, 1975; Mech,
1970; Base, 1972, 1973; Zimen, 1975).

The social organization in wolves has been particularly well
studied. In wolves, a sexually mature daughter (as judged by behavior
and vaginal bleeding) will be subordinate to her mother, and possibly
other female group members (Mech, 1970; Zimen, 1975). Her mother will
attempt to keep her from mating by aggressive intervention (Mech,
1970; Zimen, 1975).

Less information is available on the monogamous mongooses. Haas
(1972) reports that in a captive family group of the dwarf mongoose,
sexually mature daughters are subordinate to both the mother and the
father. During the breeding season, it is the father who aggressively
intervenes to prevent mating attempts between the daughter and her
brothers (Haas, 1973). Rood (1980) reports that, in feral groups

containing more than one adult female, pregnancies of subordinate

19
females do occur, but are rarely successful.

While little information is available on hylobatids, Fox (1972)
reported that, in a captive group of siamangs, a daughter who was past
the age of sexual maturity held a peripheral position in the group.
Her invitations to be groomed were always ignored, though she was the
most frequent groomer. She was prevented from feeding with the rest
of the group by aggression from her father. Her mother also displayed
aggression to her on occassion.

While much of this information is anecdotal and very little is
known about some of the species, these reports generally indicate
increased aggression to and peripheralization of young, sexually
mature females, with either the father or the mother displaying
aggression toward the daughter. In wolves and mongooses, this
aggression seemed to peak when the females of the group were in
estrus.

In callitrichids, reports of the interactions of daughters with
parents indicate a wide variety of responses. Rothe (1975) reports,
that in‘ggllighgi; ' cchus, daughters are left with their parents well
past the age of sexual maturation with no increases in agonistic
interactions. Rothe (1978) also finds that older daughters tend to
have the fewest social contacts with the parents. Other reports on
various species indicate that agonistic interactions between mother
and daughter increase as the daughter matures. Snyder (1972) observed
the formation of dominance hierarchies between Lgontgpithecus 12351;;
mothers and adult daughters with mother being dominant. Removal of
young from their parents at around a year of age has been recommended

for some species, as keeping them together longer resulted in fighting

20
between the offspring and the same-sexed parent (Lorenz, 1972,
leljgflgg gggldi; Mallinson, 1975, various Eélli£2£i£.8nd.§££2222£
species). Kleiman (1979) reports infrequent, but quite severe,
outbreaks of aggression between1Lgmggggli; mothers and daughters.

The relationship between these increases in aggression and the
daughter’s sexual maturation is unclear. The daughters in the reports
cited were older than the reported age of sexual maturation. However,
as the daughters did not reproduce and showed no external signs of
estrus, the actual reproductive state of the females in most of these
studies is not known. There is some question as to whether they were
sexually mature, despite their advanced ages (see Sggigl Igflgencgg,gg
MW)-

,Mg;§igg,§gh§zigg. Another type of social communication which
might be affected by sexual maturation is marking behavior.
Callitrichids possess highly developed sebaceous scent glands, which
are used in marking objects and occassionally other animals (Epple,
1967; Hershkovitz, 1977). Claude are concentrated in the anogenital
and sternal areas. A number of functions are attributed to this
marking, including sexual signalling (Epple, 1967; French and Snowdon,
in press), delineation of territory (Epple, 1967, 1970b; French and
Snowdon, in press) and expression of frustration or excitement (Epple,
1967; Kleiman and Mack, 1980). Expression of at least the first two
of these functions might be expected to be affected by reproductive
state. As mentioned previously, reports vary regarding whether or not
callitrichids display a behavioral estrus. There is also conflicting
evidence as to the role of marking in sexual communication. French

and Snowdon (in press) found, in Saguinus 0 di us, that the females

21
anogenital marking increases during estrus while Kleiman (1978)
reports, in ngpggpithggug‘;gg§;ig marking decreases during estrus.
There is no direct information available on the relationship between:
the hormonal changes of puberty and marking behavior. Both males and
females begin to display anogenital marking at a very early age, well
before sexual maturation (Epple, 1967, various Egllighgig and figguigug
species; Kleiman and Mack, 1980, L3,;ggglia). However, young females
generally mark.much less often than their mothers (Epple, 1967;
Kleiman and Mack, 1980).

There is more general agreement that sternal marking serves a
territorial function (French and Snowdon, in press, fighggdipgs).
Kleiman and Mack (1980) found that daughters generally did not display
sternal marking while still in their family groups, no matter what
their age. However, these females would sternal mark when removed

from their family groups or if the mother became very ill.

MWEMW

As outlined in the previous section, a female’s reproductive state
may affect her social interactions. Conversely, the type of social
influences to which a young female is exposed may also affect the rate
of her sexual maturation.

The fact that social influences may affect a female’s reproductive
state has been amply illustrated in both natural and laboratory
populations of rodents. The observation has been made that, in some
rodent species, when densities become very high, reproduction is
curtailed (Christian, 1965, 1978; Crowcroft and Rowe, 1957; Louch,

1956; Terman, 1965). This curtailment of reproduction is the result

22

of both reproductive inhibition of mature females and inhibition of
sexual maturation in young females (Christian, 1978). Christian
(1965, 1978) has hypothesized that this inhibition is the result of
the activiation of the pituitary-adrenocortical axis brought about by
exposure to the stressful situation of crowding. Increased levels of
corticosteroids have been demonstrated to bring about reproductive
inhibition (Jarret, 1965; Hagino,‘g§‘g;,, 1969; Smith, gtflalg, 1971).
but there have been a number of studies indicating that increased
adrenal activity is not necessarily linked with reproductive
inhibition in dense populations (Brain and Nowell, 1971; Bronson and
Chapman, 1968; Pasley and McKinney, 1973; Sung, g; 51,, 1977).

Reproductive state and maturation rate in female rodents may be
altered by certain types of olfactory communication. Exposure to
primer pheromones, present in mouse urine, may cause neuroendocrine
changes in a female, resulting in changes in reproductive physiology
(Leshner, 1978). When adult female mice are exposed to all-female
groups or urine from such groups, their estrus is suppressed. This
suppression usually takes the form of prolonged anestrus or
pseudopregnancy (Rogers and Beauchamp, 1976). Cowley and Wise (1972)
found that the effect of exposure to grouped-female urine on
prepubertal females was dependent upon the reproductive state of the
grouped females. Urine from virgin females delayed first vaginal
introitus of young females but urine from pregnant females had either
no effect or brought about an earlier vaginal introitus. It is
unclear as to whether this phenomenon may play a role in natural
populations with high density, in which reproduction is inhibited

(Rogers and Beauchamp, 1976).

23

Exposure to male mouse urine also influences female reproductive
state. Prepubertal female mice will display estrous cyclicity at an
earlier age when exposed to males or male urine (Kennedy and Brown,
1970; Vandenbergh, 1967, 1969). Early exposure to adult male urine
appears to initiate increases in LH levels in the prepubertal female,
which, in a matter of days, lead to adult pituitary-ovarian function
(Bronson and Desjardins, 1974). Pheromones in male urine also have
the effect of synchronizing estrus in groups of adult females exposed
to it (Bronson and Whitten, 1978).

Social interactions have been demonstrated to affect reproductive
state in female primates, also. Generally, subordinate females are
found to be reproductively inhibited. Howell (1970) found that
exposure to frequent aggressive attacks from other females or movement
out of an established social group resulted in a longer swelling phase
during the menstrual cycle of baboons. Exposure to males did not
alter the cycle. Dunbar and Dunbar (1977) found that dominant gelada
baboon females more frequently harassed subordinate females when the
subordinate females were in estrus and subordinates produced
significantly fewer offspring. They hypothesized that harassment
'during estrus causes an anovulatory cycle or spontaneous abortion.
Subordinate talapoin monkeys did not respond to exogenous estradiol
implants with an LH surge, as would be expected of normal,
reproductive females (Bowman, g; 21,, 1978). When the subordinate
females were removed from the group, they would display an LH surge in
response to estradiol. As cited previously, it has frequently been
reported that in callitrichid groups, only one female reproduces.

Abbott and Hearn (1978) and Abbott, £5 31,, (1981) found that, in

24
‘lelitgrix,j§gghgg, subordinate females never ovulated, had a reduced
LH response to LH-RH, and showed no LH surge after administration of
exogenous estrogen. These females became fully reproductive when
removed from the presence of the dominant female.

Similarly detailed information on the effects of social influences
on maturation rates in young female primates is not available.
However, Drickamer (1974) does report that daughters of dominant
female rhesus monkeys produce their first young at an earlier age than
daughters of low-ranking females.

The late maturation of females in.monogamous species (Kleiman,
1977) may be the result of social influences. There is anecdotal
evidence available from studies of wolves and callitrichids indicating
that daughters in these species may in some way be reproductively
suppressed by their mothers. Wolves generally reach sexual maturity
at around two years of age (Mech, 1970; Seal,,g§.a;,, 1979). Seal, g;
£1‘_(1979) report that the dominant of a litter of three female pups
came into estrus at a year of age, just before the death of her
mother, the alpha-female. The subordinate pups in the group did not
mature.

Young female goldenrlion tamarins (ngnggpithgcus :osalia) are
reported to be non-reproductive while housed with their parents. They
are also known to be inhibited from displaying certain adult behavior
patterns, such as sternal marking and arch-walking (Kleiman and Mack,
1980; Rathbun, 1979). However, a ten-month old female, remaining with
her natal group after her mother’s death, displayed both sternal
marking and arch-walking. Unfortunately, no data are available

concerning the reproductive state of this female, so that it is

25
impossible to determine whether this change in behavior was related to
sexual maturation.

There have been relatively few studies of callitrichids in which
the reproductive state of daughters housed with their parents has been
quantified and the available results are conflicting. Katz and Epple
(1979) report that young saddle-backed tamarin (§§ggiggg‘£2ggigglli§)
females do not display cyclic levels of urinary estrogens when housed
with their parents. However, Abbott and Hearn (personal
communication) report that young common.marmoset (Callithrix‘jggghgg)
females housed with their parents do cycle. With so little
information available, it is difficult to discern whether these
results reflect a true taxonomic difference. Also unknown is the
manner in.which young callitrichid females might be reproductively
inhibited. While pheromones in callitrichid scent marks which would
affect female reproductive state have been hypothesized (Abbott, 35
31‘, 1981) there is not evidence available to support or dispute this

theory.

CHAPTER 2
COMPARISON OF MATURATION AGE OF FEMALES

WITH MALES AND FEMALES IN NATAL GROUPS

It is hypothesized that young females housed with males will
mature at a significantly earlier age than females housed in their

natal groups.

Methods

Sgbjggtg, The subjects of this study were twelve, laboratory-born
Sgggiggg ggdipus females. The social grouping in which each subject
was housed is shown in Table 1.

Two basic social groups were studied. Seven of the females were
removed from their natal group and placed with a strange, imported
adult male. The other five females remained with their natal groups.
Figure 1 provides the ages through which each female was examined.
Females who were removed from their natal groups were placed with
adult males on the first day they were examined. In the absence of
quantitative data on maturation age for §‘_o di us, females were
paired with males in a relatively wide age range. Based upon the
maturation age of 400 days reported by Abbott and Hearn (1978) for
Callithrix jacchus and the early results of the present study, the

ages chosen for pairing females with males ranged from 294-469 days of

26

27

TABLE 1. A description of the social groupings in which the subjects
were housed. Infant < 5 months; Juvenile > 5 months but < 24 months;
Adult > 24 months.

 

 

Subject’s ‘Iggigiggglg hgusgd with Subject:
99.129119 mamas. Maw
4218 P1 Adult Male Unrelated
4204 P2 Adult Male Unrelated
4267 P3 Adult Male Unrelated
4213 P4 Adult Male Unrelated
4302 P5 Adult Mlle Unrelated
4347 P6 Adult Male Unrelated
4356 P7 Adult Male Unrelated
4054 F1 Adult Female Mother

Adult Male Unrelated

1, Juvenile-Adult Male Twin Brother

1, Infant-Juvenile Male Ybunger Brother

1, Infant-Juvenile Female Younger Sister
4238 F2 Adult Female Mother

Adult Male Father

1, Infant-Juvenile Female Younger Sister
4296 F3 **Adult Female Mother

Adult Male Father

1, Juvenile Female Younger Sister

2, Infant-Juvenile Males Younger Brothers
4334 F4 Adult Female Mother

Adult Male Unrelated

***1, Juvenile Male Twin Brother

4349 F5 Adult Female Mbther

Adult Male Father

1, Juvenile Male
2, Infant-Juvenile Males

Twin Brother
Younger Brothers

 

* designates that individual fell into both age categories during
urse of study
died when 4296 was 541 days of age
died when 4349 was 479 days of age

age.
The mated pairs (Pl-P7) were housed in hardware cloth cages,
91x91x122 cm. Females and their natal groups (Fl-F5) were housed in

cages consisting of two units, of the previously cited dimensions,

connected by a doorway. All cages contained a metal nest box and

27

28

OHAU 8259.1

 

 

 

 

 

900
Funnies With Males Females in Natal Groups
EINMhfimanm
m0 #- -
700- i; _
800- . -
3 WE- .
m P —l
200 F- "‘
at J?
.l 1
P1 P2 P3 P4 P5 P6 F1 F2 F3 F4 F5
FeHuMm Fsmmkm

Figure 1. Ages through which each female was examined.

29
wooden perches. All groups were visually isolated from each other by
metal or cardboard partitions. The temperature in the rooms
containing the cages was approximately 230C and there was a 10:14
light-dark cycle. Each room received some natural lighting through a
small window in the door. Each group was fed twice daily. The diet
consisted of high protein.monkey feed, canned diet, fresh fruit and
vegetables, mealworms, live newborn mice, and supplemental vitamins.
ygtgngiggtigg‘gf[Segual.ggtugg§igg, As stated previously,
callitrichid females appear to show no reliable external signs of
sexual maturation. There is no perineal swelling associated with
estrus and no menstruation. In addition, Hearn, gt‘alg (1975) report
that there are no reliable, cyclical changes in vaginal cytology in
mature Q‘,j§£ghug females. In the absence of these physiological
events that can be used for assessing maturation state, changes in
plasma progesterone levels was chosen as the criterion of maturation.
Each of the twelve females was bled twice weekly during the
course of the study. In addition, non-pregnant mothers and mothers in
the early stages of pregnancy in the five natal groups were also bled.
Individuals were caught in a net, in which they were weighed. The
animal’s legs were then strapped down to a Plexiglass board while the
upper part of the body was held by a caretaker. A volume of 1.0 to
1.1m1 of blood was taken from the femoral vein in a syringe containing
0.1ml of heparin. After the blood was taken, the animal was given
orally 1ml of Incremin, an iron supplement. The tamarins were clearly
stressed by the netting and by being held, but they reacted very
positively to receiving the Incremin and most grew calmer over time.

The blood was placed in a small culture tube and centrifuged at 1800xg

30
for 15 min. The plasma was removed and stored at -70°C until assayed.

{3193;355:235,Radigjgnunggggay, Radioimmunosssay is a procedure in
which radioactively labeled antigen (in this case 3H-progesterone) and
unlabeled antigen (unlabeled progesterone) compete for a fixed number
of antibody sites. The amount of radioactive antigen which binds to
the antibody will be dependent upon the amount of competing, unlabeled
antigen. When known amounts of unlabeled antigen are used, this
relationship may be quantified and applied to determining the amount
of unlabeled antigen present in an unknown.

The radioimmunoassay procedure used here followed the methods
provided by New England Nuclear Co. (Progesterone [3H]
Radioimmunoassay Pak instruction.manual). Modifications of the
general procedure were taken from Johnston and Mather (1978) and
Gibori, 3; $1, (1977). Progesterone [1,2-3H(N)] (280-420 DPM/ps) in
benzene and progesterone stock solution (200ng/ml) in
phosphate-buffered saline (PBS) were purchased from New England
Nuclear Co. Anti-progesterone-ll-BSA serum (from sheep #337) was
supplied by Dr. Gordon.Niswender, Colorado State University.

Prior to assay, the plasma samples were extracted with petroleum
ether in order to remove potential cross-reactive corticosteroids.

Due to the high specificity of the antiserum no further processing of
the plasma was necessary (see Gibori, gt_§l,, 1977, for
cross-reactivities of the antiserum). A volume of 0.1ml of plasma was
placed in a conical glass centrifuge tube along with 0.1ml of
3H-progesterone in PBS (activity: 3000 DPM/0.1 ml). This radioactive
progesterone was added to allow for determination of percent

progesterone recovered after extraction. All samples were extracted

31
twice, with an extraction consisting of the addition of 2 ml petroleum
ether followed by mixing or shaking for 30-60 sec, centrifuging for 5
min at 1600xg and decanting the ether into a borosilicate culture
tube. The ether was then evaporated under a stream of air. After
drying, the extract was redissolved in 1ml of PBS. A volume of 0.25ml
of this solution was transferred to a scintillation vial containing
10ml of scintillation solution for determination of the percent
progesterone recovered after extraction.

All assay procedures were conducted with materials either on ice
or refrigerated at 4°C. Two volumes (0.1 and 0.2m1) of the
redissolved extracts were assayed. In addition to the extracted
samples, a range of known concentrations (2.0ng/0.1m1 to 0.0ngl0.1m1)
of a standard progesterone solution were assayed. After the addition
of the samples and standards to 10x75 mm borosilicate tubes, the
volume was adjusted to 0.2m1 in all tubes by the addition of the
necessary volume of PBS. A volume of 0.1m1 of 3H-progesterone
(activity: 16700 DPM/0.1 ml) and 0.1 ml of the antiserum (diluted to
approximately 35! blank binding) was added to each tube. All samples
at both volumes and all standards were assayed in duplicate. In
addition to these, a set of duplicate tubes containing 0.1ml
3H-progesterone and 0.3ml PBS (i.e. no antiserum) was prepared for the
determination of non-specific binding.

All tubes were vortexed briefly, then allowed to incubate
overnight. After incubation, lml of a 0.252 Dextran-coated charcoal
suspension was added to each tube. Each tube was then vortexed
briefly, allowed to incubate for 5 min, then centrifuged at 1800xg for

15 min at 4°C. During the incubation period, the unbound progesterone

32
is adsorbed onto the charcoal which is spun down to form a discrete
pellet. After centrifugation, the supernatant was decanted into 20ml
vials containing 10ml of scintillation solution. The vials were
shaken then allowed to sit for approximately three hours. These vials
and those used to determine percent-recovery were each counted for 5
min under conditions optimal for tritium in a Beckman LS-3100 Series
liquid scintillation counting spectrometer.

Results were in the form of counts per minute (cpm). The cpm from
each pair of duplicates were averaged and the average cpm of the
non-specific binding tubes were subtracted from each sample average to
produce a corrected, average cpm (here termed mean cpm) for each
sample at each volume and each standard concentration. A standard
linear curve was then computed by use of the results from the standard
concentrations in the following formulae:

logit Y- a + blogX

where. losit Y- 108elY/(100-Y)l

Y- 100(mean cpm at Elmean cpm at 0.0)

x- concentration in ng
The computations were performed using O.R.A.U. computer programs CPM
and LOGIT.

‘Agggy Vgliggtion, A total of 36 assays were performed, with a
total of 692 samples assayed. The mean slope (with standard error) of
the standard curves in these assays was -2.61 : 0.02 and the
coefficient of correlation was always greater than 0.99. The lowest
detectable level was 0.4ng/0.1ml (4.0ng/1.0ml). Percentage recovery
ranged from 521 to 981 with most samples in the 70-801 range. In

addition to the plasma samples from the study subjects, each assay

33
included the extraction and assay of one water sample and two plasma

samples from each of two plasma pools, consisting of plasma taken from

female 5, diipus outside the study (Pool #1) and female ggllithgi;
jfigshgg (Pool #2). The mean cpm of the water sample was always greater

than 902 of the mean cpm of the Control standard. The pool samples
were used to determine the intra- and inter-assay variability. The
results are described in Table 2. Coefficients of variation were
determined using the methods described by Rodbard (1971). The effect
of volume an assay results was analyzed, using the 0.1 and 0.mml
aliquots from the plasma pools. The results, given in Table 2,

indicate no substantial effect of volume on assay results.

 

Table 2. Assay validation.

Withinrassay: Between-assay:

£221.! a 321221.421). s _._..(Z).c v a _.__..(1).c v

1 36 3.7 0.34 9.1 0.57 15.5

2 35 9.4 0.71 7.5 1.50 16.4
mt a m m d 7 M s

1 0.1 ml 3.8 0.25

1 72 0.2 3.6 0.23

2 69 0.1 9.6 1.60

2 69 0.2 9.1 1.80

 

‘Agglyggg, The pattern of plasma progesterone changes over time in
young females will be fully described in the Results. Young, maturing
females displayed a variety of patterns including low, fluctuating
levels and clear spikes, indicative of a normal ovulatory cycle.

These various patterns of plasma progesterone changes are similar to

34
those reported for QELliEEIiE jacchus (Abbott, 1978; Abbott and Hearn,
1978) and for young, human females (Apter and Vihko, 1977; Apter, et
al., 1978). In the present study, no female less than 357 days ever
displayed detectable levels of progesterone.

In consideration of these results, the following operational
definitions were employed:

Sexually immature- plasma progesterone levels consistently
undetectable (i.e. less than 0.4ng/0.1m1).

Sexually mature- plasma progesterone levels consistently in the
detectable range; this includes low, fluctuating levels as well as
clear ovulatory spikes.

The number of females in each maturation state (immature and
mature) at 550 days of age in each of the two social groupings
(females with males and females in natal groups) were compared, using
a Chi-square test. In addition, the mean age at which females were
defined as sexually mature was compared between females with males and

females in natal groups, using a t-test.

Bauxite
‘Fggglggflgggggd,gith Adult Mglgs, Figure 2 illustrates the changes

in plasma progesterone levels across time for the seven females who
were each housed with a strange adult male. .The graphs indicate
progesterone levels for each female from 350 to 550 days of age.
Though some were sampled at earlier and later ages, these results are
sufficient for illustrating the changes associated with maturation in
each female. All females displayed consistently detectable

progesterone levels at some point between 360 and 495 days of age.

35

Figure 2. Plasma progesterone levels of females housed with males.

 

Plasma Progesterone (tug/0.1 ml)

36

 

 

 

 

 

8 OHAU 8259.2
P19 (42181 c
” --- Missing 0m 1 “
a __ 0 Below smu- Range . A
(0.4 lug/0.1 ml) ‘ \
" 0,)» f\ q
4 _ \e—O/ \/. ""
7 M “
2 .. i ._
I
g! ............................ ~
0 1 1 1 1 1 L 1 1 1 1 1 1 1 1 1 1 1 1 L
360 380 400 420' 440 460 480 500 520 540
_ 929 (42041 c a
6 r—- ; —l
1— /.I. ..... I/‘. —
4 _ ° ./ \“/.3 _
2 _ ._
o WW1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

 

 

360 380 400 420 440 460 480 500 520 540
Age (in days)

37

 

 

 

 

 

 

 

 

 

 

8 ORAUMOJ
P39i4287l
- 0 Below Deacmble m H
(0.4 tug/0.1 ml)
8 " '-
4 — ..
-E- - -1
O
a _ l M’flfl
g (I 1 l l 1 1 1 1 f/KJ: 11, l
380 380 400 420 440 480 480 500 520 540
g ._ P49 (4213) _
E n l
a: ”' E
4 - a
2 ‘ M /\ ./ ‘
o 1 1 L L 1 1 1 1 1 1 1 '1 1° 1 1 1 L
380 sec 400 420 440 460 480 500 520 540
anlfinthnnl

Figure 2. (cont’d.)

38

ORAU 8259.2

 

P69l4302)
F oHelowDetsetsbleRanps
(Odwnflllufll

 

O
r
16“:
3/
—§.
F<
.2ll’.
g
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l l

 

 

 

1a.... mm... (119/01 mll
§
§
§
§
§
§
§
§

 

 

520 540
T'P89(43‘7) ._
6 F- ._
l— .—
4— I —1
\ e
_. M/, ,1 , _
L- “v \ /\
I .l _1
0 1 1 1°/1 1 1 ‘1 '1 1 1/ 1 ‘1" 1 1 1 1 1
360 1380 400 420 440 460 1480 500 5201 540
Aaelhidavfl

Figure 2. (cont’d.)

39

There was a great deal of variability between females in the age at
which detectable levels were initiated and the pattern of plasma
progesterone changes.

In.samples from Pl-female, there was a low rise in progesterone at
360 days. Sampling from this female ceased at 364 days and was
resumed again at 440 days. After 440 days, Pl-female displayed
consistently high levels, indicative of pregnancy. Progesterone
levels in P2-female were undetectable up to 398 days when sampling
ceased. When sampling was resumed at 472 days, P2-fema1e displayed
consistently high levels, indicative of pregnancy. P3-female
displayed undetectable progesterone levels up to 494 days, when levels
rose into the detectable range. The levels then fluctuated below
2.0ng/.1ml until 582 days when sampling ceased. P4-female began
displaying high progesterone levels, indicative of ovulation
(ovulatory spikes) immediately upon being placed with a strange male
at 469 days. Because this female was not paired with a male until
well past the earliest maturation ages seen in other females, these
results will be omitted from the determination of mean age of
maturation of females housed with males. P5-female displayed
undetectable progesterone levels up to 423 days, at which point the
levels fluctuated below 2.0ng/.1md. At 451 days, PS-female displayed
an ovulatory spike, with a peak progesterone level of 6.0ng/.1ml,
after which levels dropped again, fluctuating below 2.0ng/.1ml.
P6-female began displaying clear ovulatory spikes, with peak
progesterone values of 3.5-4.0ng/.1ml at 392 days. P6-female was
paired with a strange adult male sometime between 379-382 days and

sampling began at 385 days. It is impossible to determine her

40
reproductive state from 379-385 days. P7-female was paired with a
male at 399 days but sampling could not begin until 421 days. This
female displayed consistently undetectable levels to 463 days of age.
Levels were low and fluctuating to 491 days at which point levels
again dropped into the undetectable range and remained undetectable
until sampling ceased at 521 days. Because determination of the age
of maturation of this female is impossible from these results, she
will be omitted from further consideration.

.zgmglgg‘gggggg‘ig Natal Gggups, Figure 3 illustrates the
changes in plasma progesterone levels across time for the five females
housed in their natal groups. In some females, the first samples
assayed were when the subject was older than 350 days even though
samples had been collected at ages beginning well before 350 days.
Samples were taken and assayed from all females up to 550 days of age,
past the latest maturation age of a female with a male. Four females
(F1,F2,F4,F5) displayed consistently undetectable levels of
progesterone up to 550 days. One female (F3) displayed an ovulatory
spike of 3.0ng/.1ml at 487 days followed by low, fluctuating levels,
interspersed with more spikes up to 609 days, when sampling ceased.

Two females (F1,F2) who were still immature at 550 days were
sampled past 550 days. Fl-female displayed undetectable levels up to
666 days, at which point levels rose to 7.9ng/.1ml by 670 days.
Sampling ceased at 670 days and was resumed at 760 days, at which
point this female displayed low, fluctuating levels. Sampling again
ceased at 840 days. F2-female displayed low, fluctuating levels at
450-475 and 540-550 days, however these detectable levels were not

taken as an indication of maturation because they were interspersed

41

Figure 3. Plasma progesterone levels of females in natal groups.

42

 

 

 

 

Plasma Progesterone (no/0.1 ml)

-

—

 

°‘Y'°—1°—1°—°r°°'?—1°°f’—T°°I°°

i .
13—1! 1- 1.x: "fi/ \1/\'1/\/‘1‘/\1\‘1_'i

oeausgasa

F19l4054)
- “moat-Missing ‘
_ oHslowDetscteble Range _

(0.4nq/0.1 ml)

1.— —-
1 1 1 1 1 L 1 °1—t°°'°°"il ‘°?‘°'? i°°"1°"‘r"'Y°-‘°1 1 1
380 $0 400 420 440 460 480 500 520 540 560

_

 

szosaossovsomsooszosso

Ag (in days)

43

OHAU 8239.3

 

 

 

 

 

 

 

8
F29 (4238) a
0 Below! Detactable Range
6 _ (0.4 tip/0.1 ml) _.
4 ‘- -1
E — d
s 2 r '1
2 — [\A
3 t) l .11 l l 1 l l l 11,1L, 1, 5 1 1 1 l
g 380 3801 1400 420 440 4060 480 l3!) 520 540
g - 1
1t
6 r- .1
E
I *— —1
I
4 r— _
2 '\
M x, .
_.. l \J-cfl/ ._
0 WW 1 1 1 1 1 1 1 1 1 1 1 1 1
560 680 8001 620 (PM) 660 INN) 700 720 7W“)
A90 (in day!)

Figure 3. (cont’d.)

44

OHAU 8288.3

 

 

 

 

 

 

 

 

 

8
F39l42981
*‘ofhkwvoummmNeHpr '-
6 __ (OAmellnfll
4 - —1
'E ' ‘
i’: 1 .5
~— ,- 1.1K. .I\ f
g t) 1 1. 1 1 °1F*°?°°TT'%9°?F““T’°3. 1"? 1~ 1 1
380 3801 400 420 «440 460 4801 500 520 540
g .
d:
6 ._
4 a
4 ' —1
2—'\ / —
/“x
o 1 1'1°1 1°‘1 1 11 L 1 1 1 1 1 1 1 1 1
560 580 (NM) 620 640 660 6801 700 720 740
Agslindays)

Figure 3 (cont’d.)

45

 

 

 

 

Plasma Progesterone (nu/0.1 ml)

 

6 OHAU82II.3
F49‘4334)
I—O WM”. Range —
2 l- _l
o 1 1 1 1°°1°°1°'°°1°° °1ML° C{NEWI:o1“""1°""’1°'°°1'°°1°"""1a"
360 380 400 4201 440 460 1480 500' 5201 540
4 — _
2 - ._
0 1 L°’°'?° E°°1°°°f °°1°° T-°T °°1°° 1 °°1°°°l°°°i'°°°1°°°1°°l’°°1° 1°°'°

 

 

380 3801 400 420 440 460 480 500 EEK) 540
A00 (in days)

Figure 3. (cont’d.)

46

with periods of 60-70 days in which levels were undetectable.
FZ-female did display an ovulatory spike of 2.4ng/.1m1 at 620 days and
low, fluctuating levels to 663 days. There was no return to
consistently undetectable levels after 620 days.

‘gggpggiggg‘gfi‘Agg‘gf‘figgggggigg‘ Table 3 indicates the number of
females in each social grouping who were considered mature or immature
at 550 days of age. The proportion of mature females with males was

significantly larger than the proportion of females in natal groups.

 

Table 3. Number of females mature at 550 days.

Female maturation state

Female housed at 550 days of age:

with: immatugg Mature Total
A§§l£.!els 0 6 6
Natal Group 4 1 5
Iosgl 4 7 11

x2 - 7.54, p<.01

 

The arrows in Figures 2 and 3 labeled M indicate the age at which
each female is defined as sexually mature, according to the
operational definition given previously. The arrows labeled C
indicate age of first conception in the two females in which pregnancy
was followed to parturition (Pl,P2). A gestation period of 150 days
(Epple, 1967; Hearn, 1978) was used to compute concepton date. With
the exclusion of P4-female and P2-female, the mean with standard error
of the age of maturation is 417 : 28.6. If Pl-female and PZ-female
are included by age of first conception, the mean with standard error

is 442 + 17.3. The mean with standard error of the age of maturation

47
of the three females maturing in their natal groups is 586.7 : 53.8.
A.comparison of the mean ages of maturation indicate that females with
males do mature at a significantly earlier age than females in natal
groups (417.2 vs. 586.7, t-3.0l, p<.02; 442.6 vs. 586.7, t-3.l6,
p<.02). This test of means is a conservatively biased test of the
hypothesis, because two females in natal groups who were sampled up to
550 days and did not mature by that age were not included in the
analysis. They would also obviously mature later than any of the
females who were housed with males.

The presence or absence of the mother did not appear to be
related to the daughter's maturation rate. F3-female, who matured at
487 days, was housed with her mother continuously. FS-female’s mother
died when F's-female was 479 days of age, yet she remained immature up
to 550 days. In addition, the mother’s health and reproductive state
apparentally bore no relationship to the daughter’s maturation age.
The mothers in F2 and F5 were ill and nonrreproductive (i.e. displayed
consistently undetectable progesterone levels) when their daughter’s
were 417-663 and 373-478 days, respectively and their daughters were
either none or late-maturing. The mothers in F1, F3 and F4 were all
healthy and reproductive and their daughters included early-, late-,

and nonrmaturing females.

Disgussignlggg Conclusions
The difference in maturation age between the two types of social
groups is obvious. Females with males mature earlier than females
remaining with their natal groups. The average age of maturation of

females with males was 417 days, which is quite similar to the age of

48
first ovulation of 400 days in Q;lli§h;i§,jggghgg in peer groups
(Abbott, 1978b). Epple and Katz (1980) report much earlier ages of
first conception in Saguinug fusgicgllis females, the youngest being
211 days. These fi;,fg§ci§g;lis females were paired with males at a
much younger age than.were the fi;,gggipgg used in the present study (6
months or approximately 180 days vs. 294-469 days). This difference
may indicate that female tamarins are physiologically capable of
sexual maturation at ages even earlier than those seen in the present
study.

While females remaining in their natal groups did mature at later
ages than females with males, the fact that they did mature at less
than two years of age is of some interest. Results of studies of.§;
jgggiggllig (Kate and Epple, 1979), along with general reports that
daughters do not reproduce while in natal groups, have lent credence
to the idea that mothers physiologically inhibit their daughters’
sexual maturation. One exception to this theory has been reported by
Abbott and Hearn (personal communication) who find that Q, jacghus
daughters mature while in their natal groups. Results of the present
study also indicate that §;_gg§ipgg daughters prior to two years of
age are not completely inhibited from maturing by the presence of
their mothers. Possible inhibitions of behavioral maturation and the
relationship between behavioral and physiological maturation will be
discussed in a later section (see GENERAL DISCUSSION). Because of the
limited information available, it is unclear as to whether the results
of these various studies represent species differences or variation in
husbandry techniques and methodology.

Given that females with males did mature earlier than females in

49
natal groups, the question remains as to whether this difference
reflects male-facilitation of maturation, mother-inhibition of
maturation, or both. Much of the circumstantial evidence from the
present study weakens the theory of mother-inhibition. As cited
previously, daughters did mature in the presence of their mother, with
the earliest maturing female (487 days) being housed continuously with
her mother. In addition, the reproductive state or state of health of
the mother apparentally bore no relationship to the daughter’s
maturation rate. Finally, one female was examined for 70 days after
her mother’s death and did not mature, despite the fact that she was
well past the earliest ages at which maturation was known to be a
physiological possibility.

If the presence of a strange adult male facilitates sexual
maturation, this affect appears to require separation of the female
from her natal group as well. Two females housed with their mothers
were also housed in the presence of an unrelated adult male and these
females did not mature at the early ages of those females housed with
a male only. The fact that strange adult males in natal groups did
not accelerate maturation in young females might be related to a
number of factors. It could be that the simple presence of a strange
male does not exert a direct neural effect resulting in activation of
the pituitary-gonadal axis, as is seen in the accelerated puberty of
some rodents (Bronson and Desjardins, 1974). Perhaps certain
behavioral interactions between the male and the young female are
required for acceleration to occur. Certainly the strange males in
natal groups did not have the same types (or the same frequencies) of

affiliative or sexual interactions with the daughters as did the males

50
and young females who were paired. Despite the fact that the mother’s
presence, alone, does not seem to account for any possible delay in
daughter maturation, it might be the case that some factor or
combination or factors do serve to make the natal group an inhibiting
environment for the young females. It is impossible to determine the
validity of any of these possibilities with the information presently

available.

CHAPTER 3

BEHAVIORAL CHANGES ASSOCIATED WITH SEXUAL MATURATION

The following,§.2;ig;i hypotheses are proposed:

In pairs composed of young females and adult males, sexual
interactions will be more frequent when the female is sexually mature
than when she is sexually immature.

In pairs composed of young females and adult males, affiliative
interactions will be more frequent when the female is sexually mature
than when she is sexually immature.

When a young female stays in her natal group, the young female
will display less affiliative interactions with her mother when the
young female is sexually mature than when she is immature.

When a young female stays in her natal group, the young female
will display more agonistic interactions with her mother when the
young female is sexually mature than when she is immature.

All young females will mark more frequently when they are sexually
mature than when they are immature.

In addition, the following 3 pgsgegiggi hypothesis is proposed:

Females housed in natal groups in.which the adult male is not
their father will differ from females housed in natal groups with
their father, in terms of frequency of marking and of affiliative

interactions with their mother.

51

52
flgthods

Behagig; Observgtion . The subjects and their housing conditions
have been described previously (Table 1). On an average of three days
each week, behavior observations were conducted on all groups.
Behavior observations were never conducted during days on.which blood
was taken. Observations were conducted at all times between 0800 and
1600, with the order in which groups were observed on any given day
being random.

A single observation period of a given group lasted 20 min. The
observer would sit in visual contact with the animals at a distance of
2.0-2.4 m from the cage. After an habituation period lasting 2-5 min,
the observer would record, on a cassette recorder, all occurrences of
selected interactions, noting the performer and receiver.

In the young female~adult male pairs, all occurrences of the
following interactions were recorded:

A contacts B- A approaches B within an arm’s length and both
remain at this distance for at least 2 sec.

A grooms B- A, using hands or teeth, examines the coat or skin of
B, accompanied by visual inspection.

A sniffs B- A brings his/her face to within 1cm of B’s anogenital
area.

A nuzzles B- A rubs his/her face on B’s back or neck.

A mounts B- A grabs B around his/her torso, from behind, and
presses against B’s anogenital area.

A thrusts to B- while mounted, A performs thrusting motions with
the pelvis.

The first three behaviors (contact, groom, sniff) are considered

53
affiliative while the last three (nuzzle, mount, thrust) are
considered sexual. In addition to these, all instances of either
individual marking a cage object or another animal were noted.
Marking consisted of rubbing the anogential or sternal area against an
object or another animal. Finally, the approximate length (to the
nearest half minute) of each contact greater than 1 min.was noted.

In the young female-natal groups, the following interactions
between mothers and daughters were recorded:

A contacts B- as above.

A grooms B- as above.

A sniffs B- as above.

A grimaces/squeals to B- A, with attention to B, and the corners
of her mouth pulled back, exposing the teeth, omits a squealing
vocalization.

A cuffs B- A hits or pushes B.)

A headshake to B- A, with attention to B, turns her head from
side-to-side in a very rapid motion.

A frowns at B- A distinctively lowers the brow, while facing and
displaying attention to B.

A stands to B- A, with attention to B, stands, supporting her
weight entirely on her hindlimbs.

A chases B- self-explanatory.

A and B fight- A and B grab and bite each other.

The first three behaviors (contact, groom, sniff) are considered
affiliative while the remaining behaviors (grimacelsqueal, cuff,
handshake, grab, frown, stand, chase, fight) are considered agonistic.

As with male-female pairs, all instances of either mother or daughter

54
marking were noted, as were contact times over 1 min.

,Anglyggg:.g12;igzi hypothgse . The behavior observations on each
female were divided into two groups: those occurring when the female
was immature (i.e. when progesterone levels were consistently
undetectable) and those occurring once the female had reached the
initiation of sexual maturation (i.e. when progesterone levels became
consistently detectable). A comparison of the frequency of selected
behaviors in the immature state versus the sexually mature state was
then made. Because different females were examined across different
ages and some matured much later than others, the number of
observations of each female in each maturation state vary widely (see
Table 4) making any analyses encompassing all females impractical.
For this reason, results from each female were analyzed separately.

The method of determining whether the frequency of a behavior
varied according to maturation state depended upon the general
frequency of occurrence of the given behavior. Two behaviors, mark
and contact, occurred frequently and in most observations periods for
all groups. In this case, the data were transformed byI;:0:§ and the
mean frequency/observation period in the immature versus the mature
state was compared, using t-tests.

Most of the behaviors, including groom, sniff, cuff, and grimace,
were observed in most groups, but were infrequent, seldom occurring
more than 1-3 times in an observation period and not occurring at all
in many observations. For these behaviors, a Chi-square test was used
to determine whether the occurrence of these behaviors was independent
of maturation state. Specifically, the number of observation periods

in which the behavior occurred or did not occur in each of the two

55
maturation states was compared. In all statistical analyses,
differences were taken to be significant if p< .05.

Finally, there were behaviors, including sexual interactions,
contacts over 1 min, frown and chase, which did not occur in many
groups and were infrequent occurrences in groups in which they were
observed. While the occurrence of these behaviors in relation to
maturation state will be mentioned, there are too few data for any
statistical analyses..

‘Aeelyeee;eIeeeeegiegiwgyeeeheeiee_ The comparison within females
in natal groups used only the results from immature females, because
two of the females did not mature during the course of the study. The
type of analysis was again dependent upon the frequency of occurrence
of the behavior in question. For infrequent behaviors (groom and
sniff), the number of observation periods in which the behavior
occurred or did not occur in each of the two social states (natal
groups with fathers and natal groups with unrelated males) was
compared, using Chi-square tests. For frequently occurring behaviors-
(contact and mark) all possible pair-wise comparisons of means
(transformed by{;:0:3) for all females in natal groups were made,

using Tukey’s test.

Resul§s

legelee heused‘gjeg Adul; Males, A total of four females was used

to determine whether the frequency of sexual or affiliative
interactions varied with the female’s maturation state. P4 and P6
were omitted due to insufficient data when these females were

immature. Table 4 indicates the number of observation periods for

56

each pair when the female was immature and mature.

 

Table 4. Number of observation periods.

Number of observation periods when female:

 

$1222.12 Inmates: 1Natsrs .2252;
21 21 4o 61
22 22 35 57
23 55 36 91
24 o 36 36
25 38 4s 86
re 4 26 30
£1 46 35 81
F2 81 17 9s
33 43 44 s7
s4 *53 o 53
as 47 o 47

 

Total I 242 hours
Total used in analyses of
.e.2;ieei hypotheses - 187 hours

* Mother present in 26 periods

 

Three affiliative behaviors were examined: contact, groom and
sniff. Figures 4 and 5 illustrate the frequencies with which males
and females contacted each other within each pair. An asterisk
indicates a significant difference between the means when immature (I)
and mature (H) in a given pair. In male-initiated contacts, two pairs
showed a significant decrease when the female matured and two showed
no change. Male-initiated contacts did not increase with female
maturation. In female-initiated contacts, two pairs showed a
significant increase, one a significant decrease and one pair

displayed no change. Female-initiated contacts did not change in a

57

 

onAU 3259.4

7 1— -
'F

6 - -4

 

Number/Observation Period

 

 

 

2 ._ .J
1 P’ .—
o 1 1 1 1 1 1 1 1
I M I M I M I M
P1 P2 *P3 'P5

Figure 4. Male-initiated contact frequencies.

16

14

12

d
a

NunflannnaNmfloanflod
a:

Figure

58

 

 

 

 

 

oaau 3259.5
_ 1r -
L _
- .1 1
1 1 _
1 l I 1 1 1 1 I
I an I NI I an I I“
'91 '92 P3 '95

5. Female-initiated contact frequencies.

59

predictable direction in relation to female maturation. Grooming was
an infrequent interaction. Males groomed females in 72 of the
observations periods (21 in P1 to 142 in P5) while females groomed
males in 172 of the periods (52 in P1 to 40% in P2). Only two pairs
showed any significant relationship between frequency of grooming and
female’s maturation state. In PS, the males groomed the female less
than expected when the female was mature (12 - 5.37, p<.025) and in
P2, the female groomed the male less than expected when the female was
mature (12 I 5.23, p<.025). Sniffing was also an infrequent
interaction. Males sniffed females in 172 of the observation periods
(61 in P1 to 281 in P2). Females sniffed males in 161 of the periods
(82 in P3 to 382 in P1). No pair showed any significant relationship
between frequency of sniffing and females’ maturation. In summary,
the frequency of the three affiliative behaviors (contact, groom and
sniff) in male-female pairs did not increase when the females matured.

Three sexual behaviors were quantified: mount, nuzzle and thrust.
Successful mounts accompanied by thrusting were only observed in one
pair (P2) on two occassions, during observation periods. Mounts with
thrusting were seen in P3 on two occassions, outside of scheduled
observation periods. On two occassions in PS, the female was seen at
the doorway of the nest box, headshaking and tonguing while the male
was also in the box, a probable indication of copulation. Of these
six known and probable copulations, five occurred when the female was
immature. Unsuccessful mounting by the males occurred most
frequently, occuring in 1 observation period in P1, five periods in
P3, and 9 periods in P5. Mounting was unrelated to the female’s

maturation state. In addition to these behaviors, masturbation by the

60
P3-male was noted on five occassions, two of these being when the
female was immature and three when she was mature. These limited
observations provide no indication that sexual interactions increase
after the females have matured.

Figure 6 illustrates the frequency of female marking in each pair.
Mean.marking levels were higher in all females once they matured.

This difference was significant in 3 females.

fiegelee‘geeeee‘ielgeeel ggeues, A total of three females was used
to determine whether the frequency of affiliative or agonistic
interactions between mother and daughter varied with the daughter’s
maturation state. F4 and F5 were omitted because they did not mature
during the course of the study. Table 4 indicates the number of
observation periods for each group when the daughter was immature and
mature.

The same affiliative interactions were examined in mother-daughter
pairs as those quantified in male-female pairs: contact, groom and
sniff. Figures 7 and 8 illustrate the frequencies with which mothers
and daughters contacted each other. The only significant differences
in frequency of contacts when immature vs. mature in mother-initiated
contacts was in F2, in which contacts decreased when the daughter
matured. Two daughters (F2,F3) contacted their mothers significantly
less often once they matured. However, one daughter (F1) contacted
her mother significantly more often once matured. Grooming was
generally an infrequent interaction (see Figure 9) and with one
exception, the frequency of observation periods in which it occurred
was independent of the daughter’s maturation state. The one exception

was in F1, in.which the daughter groomed the mother more often when

61

O H AU 8253.6

 

181-

16-

.5
h
T

_s
N
\"l

I‘

NunuxwflthwwanIPafiod
m
'fi

 

 

l‘al

W

 

 

6.. —
41. -
2.. _
o ,7 1 1 1 1 1 1
1 11 I 11 1 l I“
'91 P2 “P3 *P5

Figure 6. Female marking frequencies.

62

.mmaocoavouw uomucoo
vuumwuwcwlnmuswamn .m ousmwm

was Nae was
- cs _

.mouocmsvunu uumucoo
voumauacwluunuoz .n unawwm

«a. pm

 

 

 

 

IdlE

 

 

QGDNO 3(CO

hdnflfl 3(C 0

pound uoummmwnu

63

.vouuaooo mafiaoonw noqsa cw meoauma mo unmoumm .m enough

Pm:
cc .

 

 

mm «m —m
Q‘ . gs . e‘ .

 

 
 

.rasxxzfiutmgazcfikzzbaso

 

8.285 B:E=..§=§

 

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adowa 3(‘0

cow

was Memo 10 11mm

64
mature. Sniffing was also a relative infrequent interaction. Mothers
sniffed daughters in 42 of the observation periods (12 in F1 to 72 in
F3) while daughters sniffed mothers in 332 of the periods (102 in F3
to 652 in F1). Frequency of observation periods in which sniffing
occurred was independent of maturation state in all three groups. It
is interesting to note that most instances of relatively high
frequencies of daughter-initiated affiliative interactions and any
increases in those interactions with maturation all occurred in only
one group, F1. The other two daughters displayed decreases in
contacts and no changes in grooming and sniffing frequencies with
maturation.

Two agonistic behaviors were observed across all three groups.
These were cuffing, considered aggressive, and grimacing, considering
submissive. Figures 10 and 11 illustrate the percentage of
observation periods in which these behaviors occurred. Mothers cuffed
daughters more than daughters cuffed mothers. However, there was no
relationship between the frequency of cuffing and the daughter’s
maturation state. Mothers were never seen grimacing to daughters.

All daughters displayed grimacing only when they were immature. One
daughter (F1) displayed grimacing often enough for the difference
between the immature and mature state to be statistically significant.

Other aggressive behaviors were observed only in certain groups.
Mothers were observed chasing daughters in F2 (8 observation periods)
and F3 (2 periods). Of these 10 chases, 7 were when the daughter was
immature. Frowning was only displayed by the daughter in F1. She
first frowned at her mother nine days after the mother had given birth

to the daughter's younger siblings. During this observation period,

65

 

 

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pm
5..

 

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mm «L . pm
cc . cc . cc _

 

figs :8 its:

 

 

Opdmflfl 3(‘0

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66

ORAU 8259.11

 

Percent of Observation Periods

 

 

 

*F1 F2 F3

Figure 11. Percent of periods in which the daughter grimaced.

67
the daughter frequently approached the mother and frowned at her nine
times, usually accompanied by standing and headshakes (this is also
the only time that standing was seen). The daughter frowned again at
the mother during three observation periods, though less frequently
within each period. These three periods occurred within two weeks of
each other when the mother was about midway through a second
pregnancy. No fighting was ever observed in any group.

Figure 12 illustrates the frequency of mother and daughter
marking, according to the daughter’s maturation state. The only
changes in marking behavior occurred in F1, where the mother marked
less often and the daughter marked more often when the daughter became
mature. A comparison of the daughters’ marking frequencies indicate a
similar relationship to that seen in affiliative interactions. The
daughter in F1 displayed an increase in marking and generally higher
marking levels regardless of maturation state than the daughters in F2
and F3 who marked infrequently.

The results reveal no consistent changes in the mothers’
interactions with their daughters when their daughters nature. In
terms of the daughters’ behaviors, the results from F2 and F3 were
quite consistent and indicate that daughter-initiated contacts and
possibly grimacing decrease when the daughter matures. In contrast,
the relatively rare events of grooming, sniffing and marking did not
change. The daughter in F1, however, displayed high and increasing
levels of most affiliative and marking behaviors throughout her
maturation. In an attempt to understand these differences, it was
hypothesized that the behavior of Fl-daughter could be explained by

the fact that she was housed with an unrelated male, in addition to

68

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um um was mm am pm.

ea .
m. min ..

1-0-12

HH-i-

3:
c5

 

i
I——o—-1
1
N

l
1
c
P

pow mama/mum

 

 

 

 

 

dibfln 3(CO

69

O RAU 8259.13

 

 

 

3
g
g 2 - ._
jg
$3 1 .. ..
.3
E
5 I

0 1 1 1 - 1

 

F1 F4 F2 F3 F5

Figure 13. Marking frequencies of immature daughters.

70
her mother and siblings. Two females (F1,F4) were housed in groups in
which the adult male was not their father. These males were placed in
the groups when the daughters were approximately 330 and 270 days of
age, respectively. Because F4-daughter did not mature during the
course of the study, the effect of an unrelated male vs. a father on
behavior after maturity could not be examined. However, affiliative
and marking behaviors of all immature females in natal groups were
compared in order to determine whether F1- and F4-daughters differed
from.the females housed with their fathers. F1- and F4—female did not
differ from the others in mean frequency of contacts of mother or in
percentage of observation periods in.which grooming occurred.
However, they did sniff their mothers in significantly more
observation periods (X2-18.23, df-1,p<.001). F1- and F4—daughters
also differed from those females with fathers in terms of marking
frequency. Figure 13 illustrates the mean marking frequencies of all
daughters when immature (400-620 days of age). F1- and F4-females
were very similar and differed significantly from the other three
females. It appears then that marking frequency in immature females
in natal groups may be affected by the presence of an unrelated adult

male.

Discussion.eee Conclusions
{eyeles‘geeeee‘gieg‘geleee Generally, contact frequencies did not
change in a predictable fashion when the females matured. Across
pairs, changes in contact frequencies included less contacts once the
female matured, more contacts, and no change. Grooming and sniffing,

the other affiliative interactions which were quantified, occurred

71
quite infrequently in all pairs and their frequency of occurrence
generally did not vary-with the female’s maturation state Sexual
interactions were also quite infrequent and there was no increase in
their frequency with the female’s maturation. Sexual and affiliative
interactions in young female-adult male pairs have been reported to be
infrequent in'ge.jeeegge (Abbott, 1978) and‘ge feseicellis (Epple and
Rats, 1980). In the present study, these interactions were not only
found to be infrequent, but their frequency was found to be
independent of the female’s maturation state.

The only behavior which does appear to change in frequency with
female maturation is marking. Females generally marked more
frequently once they matured.

'Eeeeleelgegeee,;eԤeeel,Ggeues, Mother-initiated affiliative
interactions with their daughters generally did not vary with the
daughters’ maturation state. It is difficult to draw any finm
conclusions concerning changes in daughter-initiated affiliative
interactions from the results of this study. Two daughters did show a
decrease in contacts of their mother once they matured, however one
daughter (F1) contacted her mother more frequently when mature.
Grooming and sniffing were relatively infrequent behaviors, the
occurrence of which was independent of the daughter’s maturation state
in two groups. However, in one group, Fl, the daughter groomed and
sniffed her mother frequently and the daughter’s grooming frequency
increased when she matured.

There is some reason to believe that the behavior of the
daughter in F1 can be partially explained by the fact that the adult

male in her natal group was not introduced to the group until she was

72
330 days of age. In a comparison among the five immature females
examined in their natal groups, females with unrelated males
introduced to the groups when the females were 9-11 months old
(F1,F4), were found to sniff their mothers significantly more often
than did females with fathers but did not contact or groom their
‘mothers significantly more often than did those with fathers.
However, one other observation may have a bearing on explaining the
behavior of Fl-daughter. In F1, the mother and the adult male
frequently remained in extended contact throughout most of an
observation period, which was not true of the mother-adult male pair
in F4. For this reason, contacts of the mother in F1 usually also
brought the daughter into close proximity of the adult male. It is
possible that Fl-daughter’s increased contacts of her mother reflect,
to some degree, increased approaches to the adult male.

There are, then, some tenable explanations for the differences
between the behavior of the daughter in F1 and the other two maturing
daughters. However, the number of females examined is so small (3) as
to make any conclusions about the basic e‘eeieei hypothesis tenuous.

In terms of agonistic interactions between mothers and daughters,
the results are more conclusive. Generally, aggressive behaviors were
limited to mothers, while daughters displayed submissive behaviors.
However, all agonistic interactions were infrequent. The frequency of
aggressive behaviors displayed by the mothers toward daughters did not
vary with the daughters’ maturation state. Daughters displayed
grimacing (a submissive behavior) only when immature. The one
exception to this pattern of agonistic interactions was the relatively

extreme aggressive displays of the daughter in F1 toward her mother

73
after her mother’s parturition and midway through the mother’s
subsequent pregnancy. These were periods in.which the mother was.
probably in either post-partum estrus or a false mid-pregnancy estrus
(see Kleiman and Mack, 1977). It should be noted that, in F3, the
mother displayed cyclical changes in progesterone levels going through
a number of periods of low progesterone after her daughter matured,
yet the daughter displayed no aggression toward her. There was no
adult male present in F3 during this period.

The frequency with which mothers and daughters marked did not vary
according to the daughter’s maturation state in two groups. In Fl,
however, the mother marked less frequently and the daughter marked
more frequently once the daughter matured. Once again, the behavior
of Fl-daughter may be related to the fact that she was in the presence
of an unrelated adult male. Immature females in natal groups with
unrelated males marked more frequently than those with fathers. The
marking frequency of these immature females in natal groups with
unrelated males was in fact more similar to the marking frequencies of
the immature females paired with males than to that of the other
females in natal groups.

The euggiegi hypotheses being tested basically proposed a
relationship between the frequency of occurence of certain
interactions involving young females and the maturation state of those
females. Generally, there was no obvious relationship between the
interactions observed and the maturation state of the females. The
course of behavioral development of females, both in male-female pairs
and in natal groups, is probably controlled by a number of

physiological and environmental factors. While the endocrine changes

74
associated with sexual maturation may affect behavior, their
occurrence, in and of itself, does not appear to initiate discernable
changes in the behaviors examined. The one exception is marking
behavior. Sexual maturation was associated with increases in marking
behavior in young females housed with males. Yet here is an example
of how other environmental factors may interact with the changes of
sexual maturation to determine behavior. While two females housed in
natal groups matured, they showed no increases in marking behavior.
However, one female housed in a natal group containing an unrelated
adult male did display increased marking when she matured. Therefore,
presence of a strange adult male may be an important factor in
determining whether increased marking will be associated with sexual
maturation. Though the evidence is much less extensive, the
aggression displayed by the daughter in F1 during her mother’s
probable estrous periods may be another example of a situation in
which the presence of a male interacts with maturation state in
determining behavior. The evidence for this argument is the
difference in the interactions of the mature daughters with their
estrous mothers in a group in which an adult male was present (F1) and

one in which an adult male was not present (F3).

GENERAL DISCUSSION

Two basic hypotheses were addressed by this study of the
cotton-top tamarin, §£8¥i£!£.2£2122£ oedieu . The first hypothesis
was that the age at which females reached sexual maturity would vary
depending upon the social enyironment in.which they were housed.
Specifically, it was hypothesized that females housed with adult males
would mature earlier than females remaining in their natal groups.

The second basic hypothesis was that certain behavioral interactions
involving young females would change in frequency when the females
matured. The results of this study will be discussed in relation to
these hypotheses and the conclusions reached will be related to what
is presently known or theorized about the social structure and
maturation processes of callitrichid females.

Any discussion of sexual maturation should be prefaced by an exact
definition of this term. Sexual maturation, or puberty, is a
prolonged process, rather than a distinct event. Any number of
histological, physiological, morphological and behavioral changes can
be used to describe it and use of different methods will provide
different assessments of when an individual is mature. In the present
study, the age at which a female’s plasma progesterone level remained
consistently in the detectable range was used as an operational
definition of age of sexual maturation. The fact that progesterone

levels consistently rose into the detectable range is an indication

75

76

that follicular maturation is proceeding to the point that
progesterone is being produced. Most females displayed progesterone
spikes that were sufficiently high to be indicative of ovulation
during the course of the study. However the relationship between the
age of the first ovulatory spike and the age of first detectable
levels of progesterone varied between females. There is also probably
a variable relationship between the age of maturation, as
operationally defined here, and the age at which a female is
physiologically capable of maintaining a pregnancy (see Vihko and
Apter, 1981).

memmmmumm In the
present study, social organization had a definite effect on sexual
maturation rates. Females housed with adult males matured at a much
earlier age than females remaining in their natal groups.

The theory that social factors can accelerate or inhibit sexual
maturation has been substantiated in a number of taxa. The most
extensively understood of these phenomena in mammals is the
acceleration of female sexual maturation in rodents by adult males
(Bronson and Desjardins, 1974; Kennedy and Brown, 1970; Vandenbergh,
1967, 1969). There is less extensive evidence that adult females may
inhibit sexual maturation in young females rodents (Cowley and Wise,
1972; Rogers and Beauchamp, 1976). While social factors are known to
affect the reproductive cycle of mature females in nonrcallitrichid
primates (Bowman,‘ee.ele, 1978; Dunbar and Dunbar, 1977; Rowell,
1970), their effect on sexual maturation appears to be unknown.

Within callitrichids, it has been hypothesized that the presence

of the mother inhibits the daughter’s reproduction (Epple 1975; Kata

77
and Epple, 1979; Lorenz, 1972; Rleiman, in press; Rleiman and Mack,
1980). Specifically, it has been hypothesized that this lack of
reproduction is due to inhibition of maturation (Kleiman, in press).

In the present study, the presence of the mother, alone, could not
account for the relatively late maturation age of the daughters. In
previous studies, the possible effect of the mother’s presence has
usually been confounded with the presence of other members of the
natal group, i.e. the father and siblings, while the effect of her
absence often is confounded with the presence of an unrelated adult
male (Ratz and Epple, 1979; Lorenz, 1972). Either of these social
factors might have an effect on sexual maturation.

Because the results of the present study, as well as those of
others, (Abbott and Hearn, personal communication), indicate that
daughters in some callitrichid species may become sexually mature
while in their natal groups, the question arises as to why these
females generally do not reproduce (Epple, 1967; Rleiman, in press;
Rothe, 1975). Two possibilities seem the most tenable. The first is
that they are physiologically inhibited at some level other than
ovulation. While young females in natal groups may experience the
initiation of sexual maturation and ovulation, they may be incapable
of supporting a pregnancy. Vihko and Apter (1981) report that, in
human females, it is a number of years after the initiation of
ovulatory cycles before cycles with normal length luteal phases are a
regular occurrence. Fertility, then, may naturally come much later
than the initiation of sexual maturation. It may also be that stress
reduces fertility in a mature daughter. It has been theorized that

inability to reproduce due to spontaneous abortions may be caused by

78
social stress in some baboon groups (Dunbar and Dunbar, 1977).

The second possibility is that young females are behaviorally
inhibited. The occurrence of an incest taboo is reported in some
species (Rothe, 1975). The exact role of each group member in
maintaining this taboo is unknown. In other monogamous species,
active behavioral inhibition of (i.e. intervention in) the sexual
activity of offspring by the parents is reported (Mech, 1970; Rasa,
1973). Intervention by parents in their offspring’s sexual behavior
is not reported to occur in callitrichids. Rather, Rothe (1975)
reports that.§§lli£h£i£.jl££h!£ females actively repel the sexual
advances of their brothers. It may be that physiological and
behavioral inhibition are both in operation. The result might be that
daughters within their natal groups seldom become pregnant and, when
they do, the pregnancies are generally unsuccessful.

The possibility that unrelated males may facilitate sexual
maturation in callitrichid females has been hypothesized (Cebul and
Epple, in press). However, as mentioned previously, in.most cases the
effect of the presence of an unrelated male on.maturation is usually
confounded with the effect of the removal of the female from her natal
group. In the present study, two females were exposed to unrelated
males while still in their natal groups and neither of these females
matured early. The lack of early maturation of these females could be
interpreted in a number of ways. As stated previously (see CHAPTER 3.
Discussion and Conclusions) it might be the case that any accelerating
effect requires certain sexual or affiliative interactions between the
male and the young female. In mature females of many mammalian

species, sexual activity can bring about endocrine changes leading to

79
ovulation (Feder, 1981). It might also be the case that the natal
group exerts some inhibitory effect that the unrelated male’s presence
does not counteract. The lack of early maturation may also simply
indicate that unrelated males do not accelerate female sexual
maturation in callitrichids, but rather the natal group has an
inhibitory effect.

Wmmwmm The
behavioral development of callitrichid females in natal groups has
been documented (Cebul and Epple, in press; Epple, 1967; Hoage, in
press; Kleiman, in press; Kleiman and Mack, 1980; Rothe, 1978) The
behavior of young females with males has also been examined (Abbott,
1978; Epple and Ratz, 1980). However, none of these studies attempted
to relate behavioral changes to sexual maturation in any form.

One of the basic hypotheses of this study was that certain
behavioral interactions involving young females would change when the
female matured. The hypothesis was addressed on a very general level.
The frequency of occurrence of selected interactions were compared
when a given female was immature and mature, with these states defined
as previously described. There was no attempt to relate behavioral
changes to any of the specific hormonal changes of puberty. Also, the
only aspect of behavior which was examined was frequency of
occurrence.

It was proposed that affiliative and sexual interactions would
increase in young female-adult male pairs when the young females
matured. The results, however, indicated no predictable change in the
frequency of these interactions relative to the female’s maturation

state. It is possible that the endocrine events of maturation do have

80
an effect on.male-female interactions, but that the change may be
quite gradual. In other primates (Goldfoot, 1977; Hanby and Brown,
1974; Wolfe, 1978) the sexual behavior of mature females does differ
from that of immature females but the changes are gradual, stretching
over many years.

The specific changes, or lack of change, in affiliative
interactions in the various pairs is interesting to note. Male
contacts of females generally did not increase when the females
matured. The two females which displayed increases in contacts of
their mates were the only two known to be pregnant during the course
of the study. Wolters (1978) notes, in‘geee‘eegieee, that male
initiations of contact behaviors are quite rare. The high levels of
contacts, indicative of mated callitrichid pairs, appear to be
primarily initiated by the female. Because female-initiated contacts
did increase in the two pregnant females, only, perhaps initiation of
pair-bonding affiliations are associated with pregnancy.

Selected interactions of mothers and daughters were also examined.
It was proposed that agonistic interactions would increase and
affiliative interactions would decrease between mothers and daughters
when the daughters matured. The results indicated that the mother’s
behavior toward her daughter was essentially unchanged by the
daughter’s sexual maturation. Though it is well-documented that
sexually mature females who are unrelated are quite aggressive toward
each other (Epple, 1970, 1975; Hampton,,ee.ele, 1966; Rothe, 1975).
sexual maturation, alone, must not necessarily lead to intra-sexual
aggression. Affiliative interactions initiated by the mother were

infrequent during the entire study and did not change in frequency

81
with the daughter’s maturation.

In the case of daughter-initiated affiliative interactions, the
variation between daughters was so extreme and the sample size so
small that any specific conclusions relative to the hypothesis would
be tenuous. The results are more consistent in the case of
daughter-initiated agonistic interactions and indicate that daughters
are generally not aggressive toward their mmthers regardless of the
daughters’ maturation state. The one exception was the occassional and
relatively severe aggression displayed by one mature daughter to her
mother, which occurred when the mother was probably in estrus.
Increases in aggression, both between mothers and daughters and
between sisters are reported to occur occassionally in association
with the mother’s estrus in Leentoeithecus :esalie (Kleiman, 1979).
However, mature daughters are not necessarily aggressive toward their
mothers during the mother’s estrus, as another mature daughter in the
present study was never seen to display aggression toward her mother,
even though her mother was known to experience several low
progesterone periods. This difference between the behavior of mature
daughters may be related to the fact that, in the group in which
aggression occurred, there was a strange unrelated male present, while
in the group with no aggression, no adult male was present. The
possible interaction between.male-presence, hormonal state, and
behavior will be discussed later.

Though small sample size hinders efforts to draw conclusions
relative to the specific hypotheses, there is one clear conclusion to
be drawn. The daughter’s sexual maturation, alone, was not related to

any consistent change in interactions between mother and daughter. If

82
the same is true for the daughter’s relationship with other family
members, sexual maturation of daughters remaining in their natal
groups could pass completely unnoticed by an outside observer if no
endocrine measures are taken.

WWMWMWM
It was initially proposed that all females would mark.more frequently
once they matured. Results indicated that females in the presence of
a strange unrelated male did mark more when mature, but females in the
presence of their natal group, alone, did not. This relationship
between increased marking and the presence of a strange unrelated male
held true whether the female was with the male, alone, or with the
male plus members of her natal group. This relationship, in
combination with the anecdotal evidence on daughter aggression during
the mother’s estrus, points to the presence of a strange unrelated
adult male as playing an important role in determining whether sexual
maturation of a female brings about changes in her behavior.

In summary, social factors do affect the age of sexual maturation
of §a2a2£§i22£ females. Females housed with males mature earlier than
females in natal groups. The presence of a reproductive mother in the
natal group is not related to the maturation age of the daughter.
However, whether the presence of the natal group,as a whole, inhibits
maturation or the presence of a strange male accelerates maturation,
or both, is still unknown. The frequency of affiliative and sexual
interactions in pairs of males and young females does not increase
when the females mature, though there is some indication of a possible
relationship between increases in female-initiated affiliation and

pregnancy. There is also generally little change in frequency of

83
affiliative and agonstic interactions of mothers and daughters with
the daughter’s maturation. However, the daughter’s behavior may
change with maturation if there is an unrelated adult male present in
the natal group. Also, only females in the presence of an unrelated
adult male displayed any increases in marking when mature. The
endocrine changes of sexual maturation may bring about changes in

behavior, then, but only under certain environmental circumstances.

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