BEHAVIORAL AND NEURAL BIOLOGY 49, 398-405 (1988)

BRIEF REPORT

Effect of Novel and Familiar Mating Partners on the Duration

of Sexual Receptivity in the Female Hamster

GILLIAN L. L. LESTER AND BORIS B. GORZALKA1

Department of Psychology, University of British Columbia, Vancouver,

British Columbia, Canada V6T 1 Y7

The lordosis duration of the female golden hamster (Mesocricetus auratus) in

response to novel and familiar mating partners was examined. In Experiment 1,
females mated to the point of sexual satiation with one male hamster, and
following its removal, showed renewed receptivity in response to the introduction
of a second male. Upon sexual satiation with the second male, females either
received a novel third male or were reexposed to the original male. Total lordosis
duration in the third bout in the group receiving a novel male was significantly
greater than in the group reexposed to the original male. In Experiment 2, the
insertion of a 1-h delay between the second and the third mating partner had no
effect on the female's responsiveness, regardless of whether the third male was
the original male or a novel male. In Experiment 3, removal of the ovaries
followed by hormone replacement treatment (40/zg estradiol benzoate, 72 h prior
to testing, and 500/xg progesterone, 4 h prior to testing) failed to alter the females'
ability to discriminate between novel and familiar mating partners. These results
demonstrate that females make clear discriminations among individual mating
partners, that this can affect sexual receptivity and will continue to do so following
a delay of at least 1 h, and that the effect is not mediated by the release of
ovarian steroids. © 1988 Academic Press, Inc

It is w e l l e s t a b l i s h e d that a s e x u a l l y e x h a u s t e d m a l e will s h o w r e n e w e d
c o p u l a t o r y a c t i v i t y w i t h a n o v e l f e m a l e p a r t n e r . T h i s is o f t e n r e f e r r e d
to as t h e " C o o l i d g e e f f e c t , " a n d first w a s d e m o n s t r a t e d e m p i r i c a l l y in
rats b y F o w l e r a n d W h a l e n (1961). R e c e n t l y , L i s k a n d B a r o n (1982)
a c c u m u l a t e d d a t a c o n s i s t e n t w i t h a C o o l i d g e e f f e c t in f e m a l e h a m s t e r s .
T h a t is, f o l l o w i n g th e f a i lu r e o f a f e m a l e to s h o w l o r d o s i s f o r 15 m i n ,
or her active rejection of a male partner, presentation of a novel male

i Please address all correspondence concerning this article to B. B. Gorzalka. This

research was supported by a Natural Sciences and Engineering Research Council of Canada
Grant to B. B. Gorzalka. The authors wish to thank Dr. D. M. Wilkie for his helpful
comments and suggestions regarding Experiments 1 and 2, and Mr. H. G, Schulze for his
technical assistance with Experiment 3.
398
0163-1047/88 $3.00
Copyright © 1988 by Academic Press, lnc
All nghts of reproduction in any form reserved.
 MATING PARTNER NOVELTY AND RECEPTIVITY 399

resulted in the reinstatement of receptivity, albeit of a shorter duration.

They further reported that following exposure to and satiety with a series
of successive partners, reintroduction to the female of an earlier-mated
male would result in his rapid or even immediate rejection. The authors
interpreted this latter finding as evidence of a Coolidge effect in the
female hamster. However, this interpretation is open to question because
the female's total lordosis duration with each successive novel male
declined dramatically with consecutive partners. Had the investigators
exposed the female instead to an additional novel male instead of the
earlier-mated male, they might still have observed a short-latency rejection.
Indeed, Carter (1973) has provided evidence that a progressive decrease
in female receptivity and an increase in fighting accompany repeated
bouts of intromissions. Thus, it is possible that the rapid rejection of the
previously mated male was a function of his temporal location in the
mating sequence, rather than his familiarity. Experiment 1 was an attempt
to distinguish between these two possibilities. Therefore, following suc-
cessive matings, female hamsters were exposed to either a novel or a
previously encountered male.
Golden hamsters were obtained from Charles River Laboratories, Que-
bec, Canada. All surgeries were performed in animals of 55-60 days of
age. Twenty males were vasectomized via bilateral ventral incisions, and
four females (designated as "stimulus females") were ovariectomized
via bilateral lumbar incisions while under light ether anesthesia. Twenty-
four intact females served as subjects. Animals were housed individually
in wire mesh cages and maintained on a reversed 12h: 12h lighting cycle
(lights off at 0800 h) at 21 + l°C. Food and water were provided ad
libitum.
Receptivity was induced in ovariectomized females via subcutaneous
injections of estradiol benzoate (Sigma; 40/zg dissolved in 0.05 cc peanut
oil, given 72 h prior to testing) and progesterone (Sigma; 500/xg dissolved
in 0.05 cc peanut oil, given 4 h prior to testing). This steroid regimen
has been found to produce the behavior most closely resembling that of
females in natural estrus (Perkins, Perkins, & Bunnell, 1984).
The estrous cycles of the intact experimental females were monitored
for the duration of the experiment, beginning 12 days prior to the initiation
of behavioral testing. Vaginal smears and external vaginal phenomena
(Orsini, 1961) were used to help predict the timing of behavioral estrus.
In order to allow the hamsters to habituate to the testing environment,
each was placed individually in the chamber for 30 min on each of 4
consecutive days preceding its day of testing. Testing was conducted in
a 54 (length) x 39 (width) x 25 (height) cm Plexiglas container, lined
with approximately 2.5 cm of San-i-cel bedding material. Free access to
food and water was available. An Esterline-Angus event recorder was
used to monitor total lordosis duration(s), the measure used to evaluate
400 LESTER AND GORZALKA

2500-

2000-
r T
7
o_
1500 -

oO 1000
0
g3
o
500 •
Legend
MALE I
MALE 2
I MALE 5
I T
NOVEL ORIGINAL
CONDITION
FIG. 1. Mean lordosis duration ( _+ standard error) of female hamsters mated until sexual
satiety with three consecutive male partners: Male l, Male 2, and either a novel third
male (Male 3) or the original male (Male 1).

sexual receptivity. Females were tested on their day of estrus during the
second half of the dark portion of the lighting cycle.
For the behavioral test, each experimental female was placed together
with a male in the testing chamber and allowed to mate until the termination
criterion used by Lisk and Baron (1982) was reached; either 15 min in
which the female displayed no lordosis in response to a persistent male,
or a submissive "tail up" reaction by the male in response to aggressive
attacks by the female. At this point, the first male was replaced by a
second male, and the mating sequence was repeated. Upon reaching
criterion with the second male, the females were assigned arbitrarily and
in equal numbers to one of two conditions: reexposure to the first male
or introduction of a third, novel male. In order to ensure that both groups
of males were equally fatigued at the start of the final mating session,
novel males had been previously paired with a highly receptive stimulus
female, during the time of the first male's interaction with the experimental
female. Male hamsters were not used again until at least a 3-day recovery
period had intervened.
Figure 1 shows the mean lordosis durations with successive males in
both the novel- and familiar-male conditions. These data demonstrate
that following sexual satiation with one male, the female hamsters showed
renewed, but lower, receptivity to a novel male. Following satiation with
the second male, the females again showed this pattern with a third novel
male. However, if the original male was reintroduced as the third mating
 MATING PARTNER NOVELTY AND RECEPTIVITY 401

partner, receptivity was absent or minimal. A X2 statistic was used to

compare the total lordosis duration in the third mating test for each of
the two groups. The data for one female were not included because she
failed to show lordosis with the second male. The analysis indicated that
when exposed to a novel third male, females spent significantly more
time in lordosis than when reexposed to an original male, X2 (1, N =
19) = 12.05, p < .001. This result suggests that the female's latency to
reject the third male is a function of the male's familiarity, rather than
of a general decrease in receptivity. The female's response to the familiar
male may be due to a short-term memory for one or more of his distin-
guishing features. Alternatively, it may be the result of the female's
sensory habituation to one or more of the various olfactory, auditory,
and visual stimuli associated with the male and involved in triggering
the sexual response. If one of these two factors is responsible for the
observed effect, then perhaps the insertion of a time interval between
satiation with the second male and reintroduction of the original male
will reveal forgetting or dishabituation. Experiment 2 was designed to
examine that possibility.
Twenty of the intact hamsters from Experiment 1 were used again as
subjects in Experiment 2. Because copulation, even in the absence of
fertilization, temporarily triggers pseudopregnancy, the neuroendocrine
events associated with pregnancy in hamsters (Diamond & Yanagimachi,
t968), Experiment 2 did not begin until 2 weeks after the end of Experi-
ment 1.
The animals were prepared for behavioral testing as in Experiment 1.
The experimental females then were arbitrarily divided into four groups
of five. The procedure was the same as that used in Experiment 1, with
the modification that for half of the animals in each condition, a 1-h
delay was inserted between the reaching of criterion with the second
male and introduction of the final male. During the delay, females rested
quietly alone in the testing chamber with the room darkened. The four
experimental conditions were as follows: delay, novel male; no delay,
novel male; delay, original male; no delay, original male.
Figure 2 shows the mean lordosis durations with successive males in
all four conditions. As can be seen, reintroduction of the original male
dramatically reduces lordosis, whether or not there is a 1-h delay. However,
a 1-h delay between removal of the second male and introduction of the
final male does not result in a marked alteration in the responses of the
females in each mating sequence condition. Data were analyzed using a
X2 statistic modification which functions as a nonparametric substitute
for the two-way analysis of variance (Wilson, 1956). The analysis indicated
a significant main effect of the sequence of males, X2 (1, N = 20) =
7.20, p < .01, but no significant main effect of delay in presentation of
402 LESTER AND GORZALKA

2500-

200O

Z
_o _T_
,,~ 1500 -
r~
i

("3 1000 -
0
/
S
500 1 Legend
[Z3 MALE 1
MALE 2
I MALE 5
0 z - L

D/N ND/N D/O ME /o

CONDITION

FIc. 2. Mean lordosis duration ( _+ standard error) of female hamsters mated until sexual
satiety with three consecutive male partners under each of four conditions: 1-h delay before
introduction of a novel third male (D/N), no delay before introduction of a novel third
male (ND/N), 1-h delay before introduction of the original male (D/O), or no delay before
introduction of the original male (ND/O).

the final male, X2 (1, N = 20) = 0.8, p > .05, and no significant interaction
between sequence and delay, X2 (1, N = 20) = .08, p > .05.
One possible mechanism by which mate novelty may affect female
receptivity is by triggering some alteration in the release of ovarian
hormones. In the hamster, it has been shown that copulatory stimuli
initiate changes in ovarian secretion (Diamond & Yanagimachi, 1968).
In the third experiment, subjects were ovariectomized in order to test
the hypothesis that ovarian hormones mediate the distinctive responses
of female hamsters to novel and familiar mating partners.
The males and stimulus females in Experiment 3 were the same as
those used in Experiments 1 and 2. Fifty-four experimentally naive females
were obtained for use as subjects. Half of these were ovariectomized
and the remainder received sham ovariectomies. One week following
surgery, the monitoring of estrous cyclicity commenced in the intact
females, as described for Experiment 1. In order to compensate for the
effects of handling, ovariectomized females were handled and treated
identically. Ovariectomized females were hormonally primed for behavioral
testing using the regimen outlined for stimulus females in Experiment 1.
To control for the potential effects of injection- and handling-induced
stress, intact females were injected on the same schedule as the ovar-
iectomized subjects with equivalent volumes of the oil vehicle. The testing
procedure was the same as that for Experiment 1, except that half of
 MATING PARTNER NOVELTY AND RECEPTIVITY 403

2000 -

15OO
J
Z

O~
Cm 1OOO -

CO
O
,.,-.,
n.-
o,
500 -

Legend
CS3 M A L E 1
MALE 2
I M A L E ,3

VN X/N Vo x/0
CONDITION
Fie. 3. Mean lordosis duration ( ___ standard error) of female hamsters mated until sexual
satiety with three consecutive male partners under each of four conditions: the females
either were intact and received a novel third male (I/N) or the original male (I/O), or
they were ovariectomized and given hormone replacement and received a novel third male
(X/N) or the original male (X/O). Hormone replacement consisted of the subcutaneous
administration of 40/xg estradiol benzoate, 48 h prior to testing, plus 500/xg progesterone,
4 h prior to testing.

the animals in each mating condition were ovariectomized. The four

experimental conditions thus were as follows: ovariectomized, novel
male; intact, novel male; overiectomized, original male; intact, original
male.
Figure 3 shows the mean lordosis duration with successive males in
all four groups. It is clear that ovariectomy has no effect on the females'
ability to distinguish between novel and familiar males. A nonparametric
two-way factor analysis using the X2 statistic (Wilson, 1956) was performed.
The data for six females were excluded from the analysis because five
females failed to show receptivity to the second male in the sequence,
and one female died during the course of the experiment. The X2 test
revealed a main effect of the novelty of the third male, X2 (1, N = 48)
= 6.76, p < .01, no main effect of ovariectomy, X2 (1, N = 48) = 0.75,
p > .05, and no interaction between sequence of males and ovarian
presence, X2 (1, N = 48) = 0.53, p > .05.
The results of these experiments suggest that the novelty or familiarity
of potential mating partners is an important determinant of the receptivity
of female hamsters. Moreover, recognition of or habituation to a particular
male is a robust effect, which shows little diminution following extensive
interactions with another male and a time delay. The results of Experiment
404 LESTER AND GORZALKA

3 suggest that copulation-induced alterations in the release of ovarian

hormones cannot account for the observed effect. It remains a possibility
that adrenal steroids are in some way involved. For example, deoxy-
corticosterone can facilitate receptivity in rodents (Gorzalka & Whalen,
1977). However, this explanation seems unlikely given that in the intact
female, ovarian output of steroids would probably be sufficiently large
to mask any alteration in the secretions of the adrenal gland.
The importance of novelty in mating partners for female hamsters may
be explained in a number of ways. One explanation relates to the habituation
of the female to the various mating-related stimuli associated with a
familiar male. By this model, the initial exposure of a female to a particular
male's sight, smell, sound, or somatosensory characteristics would produce
sensory excitation which would stimulate receptivity. However, with
repeated exposure, the same stimuli would lose their excitatory properties,
and no longer elicit the sexual response. Instead, the stimuli associated
with a novel male would be required to produce excitation. In particular,
habituation may occur with the olfactory and auditory stimuli associated
with mating in hamsters. Another possible explanation relates to the
aversive properties of copulatory stimulation. It has been shown that
lordosis duration declines in response to repeated copulatory stimulation
(Carter, 1973). Thus, conditioning to the stimulus properties (e.g., olfactory
and auditory stimuli) of a familiar male may occur, and the female may
thus find the familiar male aversive on renewed contact.
The adaptive significance of female hamsters preferring novel males
might be explained in terms of optimal reproductive strategies. Huck
and Lisk (1985b) have suggested that female hamsters take multiple
mating partners as insurance against mating with a sterile male. These
investigators have demonstrated that the probability of successful fer-
tilization by a male is reduced for each successive mating with several
female partners (Huck & Lisk, 1985a). Moreover, they have demonstrated
that when given a choice, female hamsters will, in fact, choose rested
over mated males, even when the males are anesthetized (Huck, Lisk,
Parente, & Principato, 1986). It may be the case that the female's preferred
strategy, when faced with two recently mated males is to choose an
unfamiliar male to one that she herself has mated. In this way she will
increase the probability of a fertile mating.

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 MATING PARTNER NOVELTY AND RECEPTIVITY 405

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