BIOLOGY OF REPRODUCTION 28, 823-829 (1983)

Modulation of the Estrous Cycle by Pheromones from

Pregnant and Lactating Rats

MARTHA K. MC CLINTOCK’

Department of Behavioral Sciences

The University of Chicago
Chicago, Illinois 60637

ABSTRACT

Female rats were exposed to odors from females that went through a birth cycle of pregnancy,
birth and lactation. The estrous cycle was shortened by odors from pregnant rats and lengthened
by odors from lactating rats and their pups. Changes in estrous cycle length were accompanied by
changes in the length of the luteal phase (metestrus-early diestrus). A log survivor plot demon-
strated that variation in cycle length was the result of different rates of ovulation within the popu-
lation under each condition. Neither pregnancy nor lactation odors affected the intensity or timing
of the lordosis reflex. These odors could modulate fertility and coordinate birth cycles within a
group of rats.

INTRODUCTION from females in these more prevalent reproduc-

tive conditions also alter the timing of the
Female rats can modulate the ovarian cycles
estrous cycle and thereby the opportunity for
of other female rats in their social group with
pheromones (McClintock, 1978, 1983a). Odors conception.

from diestrous females (in the follicular phase) Anecdotal observations suggest that estrous
cycles are disrupted when pregnant and lacta-
shorten the estrous cycle; odors from pro-
ting females are in a colony room (Chateau et
estrous females (in the ovulatory phase)
al., 1972; McClintock, unpublished observa-
lengthen the cycle (McClintock, submitted for
tions). However, it is not known how the
publication). In addition, females that are in
estrous cycles are altered, whether airborne
the acyclic state of persistent estrus produce
odors that induce a similar pathological state in
chemosignals mediate the putative response, or
which reproductive conditions produce the
other females (McClintock and Adler, 1978).
signals.
These airborne chemosignals may play a role
in the regulation of female fertility in a popula-
MATERIALS AND METHODS
tion of rats (McClintock, 1981, 1983b). How-
ever, as in many species, female rats do not Animals
spend a large proportion of their reproductive Female virgin Sprague-Dawley rats (cTharles River
life spans having spontaneous unfertilized Labs., 3 months of age) were housed in groups. The
ovarian cycles; they spend more time in birth colony room was lit with a reversed photoperiod
cycles of conception, pregnancy, birth, and (14L:1OD; mid-dark phase at 1300 h), ventilated with
10 room changes per hour, and maintained at 22 ±
lactation (Leslie et al., 1952; Steiniger, 1950;
2#{176}C.
Short, 1976; Altmann et al., 1977). Therefore,
in order to fully assess the role of female air- Estrous Cycle Measurement
borne chemosignals in the regulation of female Two components of the estrous cycle were mea-
fertility, it is necessary to know whether odors sured: the vaginal smear component and the lordosis
component. Beginning at 3 months of age, vaginal
lavages were taken daily at mid-dark phase to deter-
mine the length and phases
of each estrous cycle.
Vaginal lavages were continued daily for every female
Accepted November 29, 1982. (N=5 5) throughout the experiment.
Received August 10, 1982. The proportion of three types of exfoliated cells
Reprint requests: Dept. of Behavioral Sciences,
was recorded from a microscopic examination of the
The University of Chicago, 5730 S. Woodlawn Ave., wet vaginal lavage: nucleated epithelial cells (N), corni-
Chicago, IL 60637. fled epithelial cells (C) and leukocytes (L). This pro-

823
824 MC CLINTOCK

portion was used to generate nine vaginal smear types statistic (sign test). All females remained in the wind
(e.g., CN, LNC, McClintock,
N; 1978). The analysis tunnel until the females in the source box had com-
and recording of all vaginal smears were done by pleted one birth cycle (i.e., until their pups were
individuals who were unfamiliar with the working weaned). Therefore, the downwind females were ex-
hypothesis and ignorant of the particular treatments. posed to a sequence of odors from pregnancy, birth,
The phase and length of the estrous cycle was deter- and lactation (Wind Tunnel A).
mined by the sequence of these vaginal smears. This design provided two kinds of controls. 1) The
Regular 4-day cycles began with two smears that estrous cycles of the downwind females were com-
contained primarily epithelial cells (>80%) followed pared with the cycles of the other member of the
by two smears that contained leukocytes (>20%) and matched-pair living upwind, controlling for age and
were designated proestrus, estrus, metestrus and di- the effect of living in a wind tunnel. 2) The cycles of
estrus I respectively (Young et al., 1941). The fifth each female were also compared with her own cycles
day of a 5-day cycle was designated diestrus II during the pretest and at each point in the source
(Nequin et al., 1979). In cycles that were 6 days or females’ birth cycle, controlling for individual differ-
longer, an extended luteal phase (metestrus-early ences in responsiveness.
diestrus) was indicated by an uninterrupted sequence This study was repeated with another set of fe-
of smears containing leukocytes. An extended follicu- males 1 month later, but with an additional treatment
lar phase (diestrus-early proestrus) was indicated by an (Wind Tunnel B). Females in the downwind box were
uninterrupted sequence of smears containing primarily exposed to odors from diestrous females for 16 days
epithelial cells (Mandl, 1951; Nequin et al., 1979). before they were exposed to the birth cycle odors.
The lordosis component was measured by checking Diestrous odors were created by choosing females
the lordosis reflex of each female daily by manual from the colony that enter diestrus I on the following
palpation for strength (0-4) and habituation (1-2). day and putting them in the source box for 24 h. They
These scores were combined into a 9-point scale which were then removed and replaced by another set of
measured the intensity of the lordosis reflex. females that were just then entering the diestrus.
Adding exposure to diestrous odor provided a
more powerful control for the effect of living in a
Wind Tunnel
wind tunnel (which can increase cycle length; unpub-
A wind tunnel, similar in design to those described lished observations) because it delayed exposure to
by Whitten et al. (1968), and McClintock and Adler birth cycle odors by 16 days, the same duration as
(1978), was constructed from three boxes connected exposure to pregnancy odor in the first wind tunnel.
in parallel by hosing (2.4 m long, 7.6 cm o.d.). Each It also controlled for age, replicated the effect of
box (0.76 m X 0.76 m X 0.23 m) was made from diestrous odors on estrous cycle length (McClintock,
galvanized sheet metal with an airtight wood frame 1983b, submitted for publication), and provided
Plexiglass lid. A fan (Berns Airking, Model AlSO) drew another basis of comparison for the effect of birth
air through the intake valve of the first box in the cycle odors.
series, designated the upwind or control box, through
the second, designated the source box, and then
RESULTS
through the third, designated the downwind or experi-
mental box. Dampers and intake valves were adjusted
to equalize the airflow rate within the boxes. Estrous Cycle Length
Each box contained two wire cages with two to
Odors from pregnant females shortened the
three living compartments each. Smoke tests demon-
strated that the baffle in front of the intake valve estrous cycles of females living downwind, in
detected the incoming airstream so that it eddied comparison with both the cycles of the upwind
into each living compartment. The wire bottom of
control group (P0.03, sign test) and the cycles
each cage was 2.5 cm above the bedding (Sanicel, Pax-
of the experimental group during the pretest
ton Co.), which was changed twice per week in the up-
wind and downwind boxes. Bedding was changed once (P0.03, sign test; Fig. 1). The estrous cycles of
per week in the source box to create a strong non- the upwind group were not affected (P0.50,
variable odor. The clear lids ensured that the light-dark sign test).
cycle within each box was identical to that of the Diestrous odors also shortened the estrous
colony room. Food and water were available ad
cycles of downwind females (P0.3, sign test;
libitum.
Fig. 1). The effect of diestrous odors was com-
parable to that of pregnancy odors, both in this
Procedure
study and a previous study (P0.50, sign test;
The estrous cycles of each female in the colony
McClintock, 1983 b, submitted for publication).
were recorded for 1 month (pretest). At 4 months of
age, four females were mated on the same day and Odors from lactating females and their pups
then put in the source box on the sixth day of preg- lengthened the estrous cycles of females living
nancy, 16-17 days before giving birth. Twelve females downwind, in comparison with the cycles of
with 4- and 5-day estrous cycles were also put in the
the upwind control group (P0.05, sign test)
wind tunnel: six in the upwind box and six in the
and the cycles of the downwind group during
downwind box. The upwind and downwind females
were paired (matching for living compartment and exposure to pregnancy odor (P0.004, sign
cycle type), permitting the use of matched-pair test; Fig. 1). The estrous cycles of the upwind
 BIRTH CYCLE PHEROMONES AND ESTROUS CYCLE LENGTH 825

I
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a 7.0
z
w
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w 6.0
PRETEST BIRTH CYCLE
-J--
0(/)
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5.0 od

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4.0 I
r

-16 -12 -$ -4 0 .4 .6 .12 #{176}16.20 .24 .26

1’
PREGNANCY BIRTH LACTATION

BIRTH CYCLE ODORS

FIG. 1. Effect of odors from pregnant and lactating females on the estrous cycle length of females living
downwind (mean ± SEM). Females were group-housed during the pretest (N=12; 16 days); diestrous odors were
only presented to females in wind tunnel B (N6; 16 days).

group were not affected (PO.12, sign test). In A log survivor plot of these data (Fagen and
addition, the estrous cycles of females exposed Young, 1978) indicates that the upwind fe-
to lactation odors in the first wind tunnel were males, exposed only to background odors, had
longer than those of females exposed to preg- a unimodal distribution of estrous cycles in
nancy odors in the second wind tunnel, when which 4-day through 7-day cycles were equi-
the two groups had been in the apparatus for probable (indicated by the straight slope of
the same length of time (P0.05, Mann- curve B in Fig. 2). Pregnancy odors increased
Whitney U test). the probability of 4-day cycles (indicated by
the steeper slope of curve A in Fig. 2). On the
other hand, the estrous cycles of females ex-
posed to lactation odors formed a bimodal dis-
tribution: one population of 4- to 5-day cycles
and a second of 9- to 16-day cycles (separated
by the plateau in curve C, in Fig. 2). Two-
thirds of the responsive females had at least one
long cycle in the second population. These
longer cycles were as likely to occur imme-
diately after the source females gave birth,
early in lactation, as they were after the source
females had been lactating for 2 weeks.

Length of Estrous Cycle Phase

Lactation odors consistently increased cycle

1234567891011121314151617 length by extending the sequence of leukocytic
TIME smears (luteal phase; 89% of cycles > 6 days
ESTROUS CYCLE LENGTH (DAYS) long). The pregnancy odors did not signifi-
FIG. 2. A log survivor plot of estrous cycle length cantly alter the length of either leukocytic
during exposure to birth cycle and background odors. smear sequences (luteal phase) or epithelial
The slope of the line at time t is proportional both to smear sequences (follicular phase). Nonetheless,
the probability of each estrous cycle length and to the
since it was leukocyte smear sequences that
rate of ovulation in the population. The arrows high-
light the lower probability of 6-8 day cycles, indi- were prolonged in non-4-day cycles during the
cating a biomodal distribution of cycle lengths. pretest, it appears that pregnancy odors re-
826 MC CLINTOCK

duced the probability of long cycles by shorten- 1971), a change in cycle length corresponds to
ing the luteal phase. a change in ovulation rate. Changes in ovula-
tion rate in the population during exposure to
Lordosis Reflex pregnancy and lactation odors are indicated
graphically by the different slopes of log sur-
The intensity of the lordosis reflex increased
vivor plots of estrous cycle length. Pregnancy
steadily from the time that the females entered
odors increased the rate of ovulation by in-
the wind tunnel whether they were upwind or
creasing the probability of 4-day cycles. Lacta-
downwind of the odor source (Fig. 2). None of
tion odors decreased the rate of ovulation by
the odors from the source box affected the rate
increasing the probability of longer cyc’es.
at which this change occurred (P0.5O, sign
Although the variability in cycle length was also
test). The increase in intensity was simply a
increased by lactation odors, it is important to
function of time spent in the wind tunnel and
note that there was structure to the variability.
not the time of exposure to birth cycle odors
The straight slope of the log survivor plot be-
(Fig. 3).
tween 9 and 16 days indicates that ovulation
occurred at a constant rate even though this
DISCUSSION
rate was random with respect to time.
Pheromones from pregnant rats shortened Variation in cycle length during exposure to
and regularized the estrous cycle. Pheromones birth cycle odors was associated with variation
from lactating rats and their pups had the oppo- in the length of the leukocyte smear sequence.
site effect; they lengthened the estrous cycle Leukocytic smears are associated with proges-
and increased its variability. Since ovulation is terone production from corpora lutea (Parkes,
indicated by the transition from cornified 1929; Hoffman and Schwartz, 1965; Damber et
epithelial cells to leukocytes in the vaginal a!., 1981). Therefore, it is hypothesized that
smear cycle (Schwartz, 1964; Weick et al., birth cycle odors alter cycle length through the

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FIG. 3. The intensity of the lordosis reflex of females living in the upwind boxes (N=6) and downwind boxes
(N..’6) and downwind boxes (N6) of wind tunnels A and B (12-day moving averages). The reproductive condition
of the females in the source boxes is indicated at the bottom of the figure.
 BIRTH CYCLE PHEROMONES AND ESTROUS CYCLE LENGTH 827

neuroendocrine mechanisms that regulate the different from those produced during the
life span of the corpus luteum. This hypothesis estrous cycle even though their effects are
is supported by the observation that proges- similar. One such candidate is the maternal
terone production is more protracted during pheromone which is a prolactin-dependent
5-day than 4-day cycles (Nequin et al., 1979). chemosignal produced by a lactating mother
Birth cycle odors did not affect the lordosis (Leon and Moltz, 1971). This maternal phero-
component of the estrous cycle. The intensity mone, which attracts pups, may also lengthen
of the lordosis reflex increased steadily from the estrous cycle of females living with her.
the time that females were separated by wire However, the maternal pheromone is not fully
mesh in the wind tunnel compartments. There- effective until 14 days postpartum and this
fore, these airborne chemosignals affect the study indicates that the estrous cycle can be
neuroendocrine mechanisms of the vaginal com- disrupted by odors from mothers and their
ponent of the estrous cycle specifically, with- pups immediately after birth. Nonetheless, the
out affecting the lordosis component. This is regulatory mechanisms of the estrous cycle
consistent with previous reports that the lordo- could be more sensitive to the maternal phero-
sis reflex of socially isolated females is un- mone than the pups are. The odor source could
affected by either olfactory communication also be the pups themselves. Contact with new-
with a group of mature females (McClintock, born pups lengthens the estrous cycles of
1981) or separate odors from each phase of the virgin females (Marinari and Moltz, 1978), an
estrous cycle (McClintock, 1983a). effect that this study suggests may be caused
Because the birth cycle has neuroendocrine by chemosignals that are either produced or
mechanisms in common with the estrous cycle, carried by the pups.
it was hypothesized that the airborne chemo- Birth cycle pheromones could serve the
signals produced during the birth and estrous function of coordinating births within a group
cycle would be similar (McClintock, 1981). of females, reducing variance in the age of
These data confirmed the hypothesis, suggest- offspring and increasing opportunity for
ing that the odors with similar effects might cooperation in their care. Odors from pregnant
have similar neuroendocrine mechanisms. The females increase the probability that other fe-
effect of odors from pregnant females was com- males will come into estrus and also become
parable to the effect of odors from females in pregnant. Odors from lactating females, how-
the follicular phase of the estrous cycle. In both ever, delay estrus, reducing the probability that
of these reproductive conditions estrogen is other females will conceive until the lactating
rising (Butcher et a!., 1974; Bex and Corbin, females have weaned their pups and can also
1981), suggesting that there are estrogen- conceive. For example, when births are syn-
dependent compounds that shorten the estrous chronized within a group of band mongooses
cycle. The effect of odors from lactating fe- (Helogale parvula), females cooperate in the
males and their pups was comparable to the care of the young (Rood, 1980). A similar pat-
effect of odors from females in the ovulatory tern may occur in rats, facilitated by birth cycle
phase of the estrous cycle. Prolactin is high in pheromones. Several females with young are
both of these reproductive conditions often found within a rat burrow (Calhoun,
(Wiersma, 1981; Taya and Sasamoto, 1981), 1962) and will pool unweaned litters (Lee and
suggesting that there are prolactin-dependent Moltz, in preparation; McClintock, unpub-
compounds that lengthen the estrous cycle. lished observations). This reduces the time that
Progesterone cannot be sufficient as a mecha- a female spends caring for her young (Lee and
nism because levels are high during both preg- Moltz, in preparation).
nancy and lactation, when different chemo- Birth cycle odors may also mediate a correla-
signals with opposing effects are produced. tion between social status and fertility. In
Furthermore, odors from metestrous females several mammalian species, fertility is sup-
(in the luteal phase) have no effect (McClin- pressed by socially dominant females [naked
tock, 1983a, submitted for publication). mole rat, Heterocephalus glaber (Jarvis, 1981);
Luteinizing hormone and follicle-stimulating marmoset, Callitbrix jacchus (Abbott and
hormone also can be ruled out as they are low Hearn, 1978). rhesus monkey, Macaca mulatta
during pregnancy and lactation (Taya and (Drickamer, 1974); reviewed by McClintock
Sasamoto, 1981;Smith, 1981). (1983b)]. If a dominant female is the first to
Nonetheless, birth cycle pheromones may be bear young, the fertility of subordinates may
828 MC CLINTOCK

then be suppressed by signals derived from her mone-releasing hormone (LHRH) and LHRH

reproductive condition rather than her domi- against termination of pregnancy in hypophysec-
tomized rats: extrapituitary site of action. Endo-
nance status.
crinology 108:273-280.
The effect of birth cycle odors has only been Butcher, R. L., Collins, W. E. and Fugo, N. W. (1974).
examined directly in one other species. In the Plasma concentration of LH, FSH, prolactin,
mouse (Mus musculus), odors from lactating progesterone and estradiol-17 throughout the
4-day estrous cycle of the rat. Endocrinology 94:
females enhance fertility; the number of days
1704- 1708.
of ovulation and estrus within a cycle is in- Calhoun, N. B. (1962). The Ecology and Sociology of
creased, although the length of the cycle is not the Norway Rat. USPHS Publication No. 1008.
changed (Hoover and Drickamer, 1979). The Chateau, D., Roos, J. and Aron, C. (1972). Action de
onset of puberty is also accelerated (Drickamer I’urine male ou femelle provenant de rats nor-
maux on castres sur Ia duree du cycle oestral
and Hoover, 1979). In this species, the effect of
chez Ic ratte. C. K. Seances Soc. Biol. Fil. 166:
estrous cycle odors is also opposite to that of 1110-1113.
the rat, females that live in a group are sup- Damber, J. E., Janson, P. 0., Axen, C., Selstam, G.,
pressed rather than enhanced (Whitten, 1959; Cederblad, A. and Ahren, K. (1981). Luteal
McClintock, 1981). blood flow and plasma steroids in rats with cor-
pora lutea of different ages. Acta Endocrinol. 98:
In the gerbil (Meriones unguiculatus), the
99-105.
effect of signals from a lactating female are Drickamer, L. C. (1974). A ten-year summary of re-
similar to those in the rat. The fertility of production data for free ranging Macaca mulatta.
daughters is suppressed if their mother is lacta- Folia Primatol. 21:61-81.
Drickainer, L. C. and Hoover, J. E. (1979). Effects of
ting. Once their mother has resumed spontan-
urine from pregnant and lactating female house
eous estrous cycles, the daughters become mice on sexual maturation of juvenile females.
fertile (Payman and Swanson, 1980). However, Dev. Psychobiol. 12:545-551.
it is not known whether the signal that induces Fagen, R. M. and Young, D. Y. (1978). Temporal pat-
terns of behaviour: durations, intervals and
the suppression is an airborne chemosignal.
sequences. In: Quantitative Ethology (P. N.
The effect of pregnancy odors does not
Colgan, ed.). J. Wiley & Sons, New York, pp. 79-
follow the same pattern across species. Preg- 114.
nancy odors increase fertility in both the rat Hoffman, J. C. and Schwartz, N. B. (1965). Timing of
and the mouse (Hoover and Drickamer, 1979) post-partum ovulation in the rat. Endocrinology
76:620-625.
and yet in the gerbil, signals from pregnant
Hoover, J. E. and Drickamer, L. C. (1979). Effects of
females do not have a strong effect on female urine from pregnant and lactating female house
fertility (Payman and Swanson, 1980). This mice on oestrus cycles of adult females. J.
diversity emphasizes that birth cycle odors can Reprod. Fertil. 55:297-301.
Jarvis, J.U.M. (1981). Eusociality in a mammal:
regulate female fertility in a variety of ways
cooperative breeding in naked mole-rat colonies.
which will depend on the specific social struc- Science 212:571-573.
ture, mating system and ecology of the species Leon, M. and Moltz, H. (1971). Maternal pheromone:
from which the domestic strains were derived. discrimination by preweaning albino rats. Phys-
iol. Behav. 7:265-267.
Leslie, P. H., Venables, U. M. and Venables, L. S.
ACKNOWLEDGMENTS
(1952). The fertility and population structure of
This work was supported by grants from the the brown rat (Rattus norvegicus) in corn-ricks
National Science Foundation 80-19496 and the and some other habitats. Proc. Zoo!. Soc. Lond.
National Institute of Aging PHS 5 R23AG02408. I am 122:187-238.
indebted to T. Butler, K. B. Church, S. Cogswell, C. Mmdl, A. (1951). The phases of the oestrous cycle in
Hedricks, J. LeFevre and D. Wolf for invaluable discus- the adult white rat. J. Exp. Biol. 28:576-585.
sions and data collection and to T. Butler for graphics. Marinari, K. T. and Molts, H. (1978). Serum prolac-
tin levels and vaginal cyclicity in concaveated and
lactating female rats. Physiol. Behav. 21:525-
REFERENCES
528.
Abbott, D. H. and Hearn, J. P. (1978). Physical, hor- McClintock, M. K. (1978). Estrous synchrony and its
monal, and behavioral aspects of sexual develop- mediation by airborne chemical communication
ment in the marmoset monkey, Callitbrix jac- (Rattus norvegicus). Horm. Behav. 10:264-
cbus. J. Reprod. Fertil. 53:155-166. 276.
Altmann, J., Altniann, S., Hausfater, G. and Mc- McClintock, M. K. (1981). Social control of the ovar-
Cuskey, S. A. (1977). Life history of yellow ian cycle and the function of estrous synchrony.
baboons: physical development, reproductive Am. Zool. 21:243-256.
parameters, and infant mortality. Primates 18: McClintock, M. K. (1983a). Synchronizing ovarian and
315-330. birth cycles by female pheromones. In: Chemical
Bex, F. J. and Corbin, A. (1981). Luteinizing hor- Signals in Vertebrates (D. MUller-Schwarze and
 BIRTH CYCLE PHEROMONES AND ESTROUS CYCLE LENGTH 829

K. M. Silverstein, eds.). Plenum Press, New York 3-24.

(in press). Smith, M. S. (1981). The effects of high levels of pro-
McClintock, M. K. (1983b). Pheromonal regulation of gesterone secretion during lactation on the con-
the ovarian cycle: enhancement, suppression and trol of gonadotropin secretion in the rat. Endo-
synchrony. In: Pheromones and Reproduction in crinology 109:1509-1517.
Mammals (J. G. Vandenbergh, ed.). Academic Steiniger, F. (1950). Beitrag zur Soziologie und
Press, New York (in press). sonstigen Biologic der Wanderatt. Z. Tier-
McClintock, M. K. and Adler, N. T. (1978). Induction psychol. 7:356-379.
of persistent estrus by airborne chemical commu- Taya, K. and Sasamoto, S. (1981). Changes in FSH,
nication among female rats. Horm. Behav. 11: LH and prolactin secretion and ovarian follicular
414-418. development during lactation in the rat. Endo-
Nequin, L. G., Alvarez, J. and Schwartz, N. 8. (1979). crinol. Jpn. 28:187-196.
Measurement of serum steroid and gonadotropin Weick, R. F., Smith, E. R., Dominguez, R., Dhariwal,
levels and uterine and ovarian variables through- A.P.S. and Davidson, J. M. (1971). Mechanism
out 4 day and 5 day estrous cycles in the rat. of stimulatory feedback effect of estradiol ben-
Biol. Reprod. 20:659-670. zoate on the pituitary. Endocrinology 88:293-
Parkes, A. 5. (1929). The functions of the corpus 301.
luteum. I!. The experimental induction of Whitten, W. K. (1959). Occurrence of anoestrus in
placentomata in the mouse. Proc. R. Soc. Lond. mice caged in groups. J. Endocrinol. 18:102-
B Biol. Sci. 104:183-188. 107.
Paymen, B. C. and Swanson, H. H. (1980). Social Whitten, W. K., Bronson, F. H. and Greenstein, J. A.
influence on sexual maturation and breeding in (1968). Estrus-inducing pheromone of male
the female mongolian gerbil (Meriones unguicula- mice: transport by movement of air. Science
tus). Anim. Behav. 28:528-535. 161: 584-585.
Rood, J. P. (1980). Mating relationships and breeding Wiersma, J. (1981). A detailed characterization of pro-
suppression in the dwarf mongoose. Anim. lactin secretion patterns during daylight in
Behav. 28:143-150. individual cycling and pseudopregnant rats.
Schwartz, N. B. (1964). Acute effects of ovariectomy Neuroendocrinology 33:288-294.
on pituitary LH, uterine weight, and vaginal Young, W. C., Boling, J. L. and Blandau, R. J. (1941).
cornification. Am. J. Physiol. 207:1251-1259. The vaginal smear picture, sexual receptivity and
Short, R. V. (1976). The evolution of human repro- time of ovulation in the albino rat. Anat. Rec.
duction. Proc. R. Soc. Lond. B. Biol. Sci. 195: 80: 37-45.