Anestrus

The anestrous female may rebuff an approaching tomcat by hissing and striking out. If she accepts the tomcat with relative indifference, she flexes her spine when he mounts and covers the perineum tightly with her tail, almost achieving a sitting position instead of the lordosis seen during estrus. The same behavior is exhibited by prepubertal kittens weighing more than 1500 g when mounted by a male. Kittens weighing less than 1000 g remain passive to the neck grip because it resembles the carrying grip used by the queen.⁸¹ The anestrous female also exhibits aggressive behaviors in attempting to free herself from an undesired mounting. Olfactory signals from her vulvar area apparently are repulsive to some tomcats, which will quickly turn away after smelling her perineum.⁸¹

Proestrus

The onset of estrous behavior may seem rather sudden to the owner because of a relatively short proestrous phase. Proestrus lasts between 1 and 3 days, and the associated behavior is highly variable among individuals. Only 16.1% of cats show proestrus.¹⁰⁵ For these, it typically begins as a subtle increase in general activity and progresses to increased rubbing against objects, especially with the head and neck. This behavior may prompt owners to report that their cat has become friendlier. A tomcat’s approach no longer results in immediate sexual aggression by the female. The male cat’s neck grip and mount may initially cause the female to crouch partially and tread temporarily. His advances during proestrus eventually initiate her aggression. During this time owners may witness more aggressive interactions between the male and female than between tomcats.²⁰ Amicable behaviors are also more often initiated by the female, and she is more likely to interact with a male that she knows.²⁰ Her rubbing the chin and cheek on objects, including the tomcat, becomes very marked within 36 hours of the onset of proestrus, and when done to a person, it may be related to courtship rather than marking.²⁴ Rubbing progresses to rolling, either gentle or violent, which is usually associated with purring, rhythmic opening and closing of the claws, squirming, and stretching^81,111 (Figure 6-1). Catnip may evoke a somewhat similar behavior.

Figure 6-1 The characteristic rolling behavior of proestrus and estrus.

The female begins calling to a male using the “heat cry,” a vocalization unique to proestrus and estrus. This sound is a monotone howling that lasts up to 3 minutes at one time. Approximately 12% of the females eventually call continuously, although this behavior is more prevalent in Siamese females. Another 14% vary considerably in the frequency of the call.⁵⁸ Some estrous females apparently do not call at all.²⁰ This cry is mimicked by the tomcat, answered by the female, and again mimicked by the male. The female may spray urine,⁸ so that both the urine and the sebaceous secretions left by rubbing serve to attract males, particularly in areas where cats live relatively close together.^24,116

Estrus

As the female enters estrus, a dramatic change occurs in her behavior toward the male. She still rolls and rubs, but no longer does she aggressively refuse the male’s attempts to mount, exhibiting a crouching lordosis instead. In this position the ventral thorax and abdomen touch the floor, and the perineum is elevated because the hindlimbs are positioned caudal to the body and extended perpendicular to the ground (Figure 6-2). This copulatory stance can be induced by stroking the queen’s back, thighs, or neck. Her tail is laterally displaced, and there may be a small amount of sanguineous discharge on the vulva.¹¹¹

Figure 6-2 The natural lordosis posture of an estrous cat.

The behavioral events of mating begin with appetitive sexual behavior, or courtship. The elaborate courtship behaviors are important to bring males and females together. To ensure that males will be available and can succeed in intermale competition (although the winner may not be the one she eventually chooses) the female starts advertising before she is fully receptive. This courtship period also helps give the greatest number of healthy males an equal chance at reproduction.⁷⁰ The female usually sits some distance away from the competition. She may show preference or dislike for an interested male. This choice probably has an olfactory basis, because changes in the nasal mucosa occur in association with the estrous cycle.⁸⁴ Evidence indicates that odors affect reproduction in several mammals by means of the nervous and endocrine systems, and theories to the contrary fail to take the learning process into account.^84,114

Lordosis is necessary if intromission is to occur and can be stimulated by the treading of the mounted male. While the male performs copulatory thrusts, the female adjusts her position slightly by alternate treading with her hindlimbs. During estrus, this rhythmic step, tail deviation, and rolling can be initiated by gently petting or tapping the female’s perineum, flank, or back (Figure 6-3). The facial expression associated with mating is often intense, similar to that seen in aggressive cats and some that are fearful. In addition, the ears are positioned rostrolaterally. The crouching, rubbing, rolling, and treading portions of courtship last between 10 seconds and 5 minutes, tending to be shorter with repeated breedings.^5,31

Figure 6-3 Estrous behavior can be stimulated by petting.

Postmating behavior of the female is characteristically dramatic. As the male starts to withdraw his penis after ejaculation, the female’s pupils suddenly dilate. Immediately after, 53.8% of queens will utter the copulatory cry, a shrill piercing vocalization.⁹⁶ Then 76.9% of queens will turn aggressively on the male.⁹⁶ To a familiar male, the female may be less aggressive and might instead proceed directly into the “afterreaction.” During the afterreaction, the consummatory portion of the female’s sexual behavior, she again rolls on the floor, stretches, and licks her vulva (Figure 6-4). This period lasts from 1 to 7 minutes.⁶⁸

Figure 6-4 The female licks her external genitalia following mating.

Typical estrous mating behavior resumes in 11 to 95 minutes (mean 19 minutes). Experienced pairs may mate as frequently as 8 times in 20 minutes, or 10 times per hour.^5,30,31 Female cats have been known to mate more than 50 times during an estrous period.⁵¹ As mating continues over the next few days, the refractory period (the time between these behaviors) becomes longer. The female mating interval, however, actually decreases, and she becomes more active in encouraging the male to mount. This is particularly true of naive females.¹²² Thus the male is primarily responsible for the increased time lapse between breedings. An estrous female can be conditioned to assume the estrous posture whenever she is placed in the mating area, even in the absence of a male.^81,122

A mutual attraction between tomcat and queen can last for extended periods. A female will generally accept a number of males during her estrous period, and many litters have multiple sires.^24,26,30 If there is a central tomcat, he is the primary breeder of that female group, even with other peripheral males courting the females.⁷² This is because of his proximity to the queens. He is not likely to fight off other males though, because it would be too dangerous for any one male to attempt to keep them all away.⁸⁵ When females are in the proximity of related males, they are more likely to leave their home areas during estrus than are those without related males nearby.⁷³

The cat is an induced ovulator, so an estrous female generally does not ovulate unless mating occurs. Ovulation occurs approximately 24 hours after copulation—the same amount of time needed for sperm to capacitate.⁸⁵ The ovulation is probably induced by vaginal stimulation from the male’s penile spines or by artificial means, such as with a glass rod. More than one natural mating may be necessary for conception.¹⁰⁴ Artificial stimulation requires several insertions of approximately 10 seconds in duration, 5 to 10 minutes apart, over a 48-hour period. Successful stimulation by either method causes the typical postcopulation aggression. The number of ovulation sites on the ovary varies directly with the number of matings and can include as many as 86.6% of the follicles with repeated matings.¹²⁴ All eggs leave the ovary at the same time.²⁶

Ovulation has been prevented by a systemic shock factor such as abdominal surgeries but only if the shock occurs within 55 minutes after mating.²

The female remains in estrus for 2.5 to 11.1 days (range 2 to 19 days), a period that may include proestrus and metestrus.^96,105 She is most receptive on the third and fourth days if mated during that time. Estrus ends rather abruptly, within 24 hours after coitus. If pregnant, the cat usually will not return to estrus again until the next seasonal peak or the next year. However, about 10% of the pregnant queens display estrous behavior and produce a vaginal smear typical of estrus during the third to sixth week of gestation, possibly because of estrogen secretion by the placenta.^3,102,109 Mating at this time can result in superfetation.^57,109 Nursing queens have also been known to exhibit estrus 7 to 10 days after parturition, but estrus generally does not occur during lactation, so most do not return to estrus until 6 to 8 weeks after giving birth. It can be delayed as long as 21 weeks.^58,102 Postpartum estrus has a shorter duration than the initial estrus, averaging 3.8 days.⁹⁹

When no tomcat is present, the female remains in estrus for 10 to 14 days, although the first estrus might last only 5 to 10 days.⁵¹ She returns to estrus in 9.0±7.6 days (range 5 to 22 days).¹⁰⁵ Some studies suggest a minimal difference between bred and open estrus duration.^96,105 The average estrous cycle is 21 to 29 days long, but it can vary from 5 to 73 days. Young females tend to exhibit minimal estrous signs; become hyperexcitable, anorectic, or withdrawn; and have a shorter estrous period. In contrast, older females continue to cycle, even though the interval between estrous periods might increase and duration and intensity of estrous behavior decrease. Approximately 35% of the time, ovulation will occur without coitus.⁶⁶ In such a cat or in one that mated but did not conceive, the luteal phase will last 30 to 36 days and the interestrous interval is 35 to 76 days.^96,105,124

Because some of the environmental factors that affect the onset of puberty in the female can also affect the onset of estrus, the nonpregnant female has been described as being in “potential” estrus during the mating season.^30,31 The result of exposure to certain factors, such as a tomcat or other cycling females, is the appearance of proestrus and estrus within a few hours to 3 or 4 days and a synchronization with female groups.^22,72,73 Valeric acid is plentiful in vaginal secretions during estrus and may be associated with the synchronization.¹¹ Other factors, such as a colony relocation, can result in coordinating estrous cycles for 42% to 77% of the females.¹²³

Estrous behavior has been controlled with vasectomized male cats. In females mated to such tomcats, estrus lasts approximately 7 days and is followed by a 36- to 44-day interestrous period of pseudopregnancy.^31,69,86,93

The behavior of a female cat, her vaginal smear, and her phase in the reproductive cycle are very closely correlated. Of the cats exhibiting estrous behavior in one study, 78% had a fully cornified estrous vaginal smear and another 18% were in proestrus.⁸¹

Metestrus

The behavior of metestrus begins with the appearance of leukocytes in the vaginal smear.⁸⁰ This phase rarely lasts more than 24 hours and is generally included in time ranges given for estrus because all of the postural responses continue and mounting is allowed. The female aggressively rejects the male during this phase only when he attempts intromission.

Contraction phase

During the first phase, contraction, the queen spends a great deal of time licking herself or the newborns already delivered. The abdominal musculature shows obvious contractions, which are considered to accompany uterine contractions. Pelvic limb movements by the queen should help distinguish these abdominal contractions from fetal movements.¹⁰⁰ Other signs of restlessness are obvious. In addition to squatting and scratching, the queen may circle, rearrange bedding, roll, or rub. She generally appears uncomfortable and seems to be constantly trying to adjust for some disturbance at the caudal portion of her body, even bracing her body against various objects. The duration of the contraction phase is variable, ranging from 12 seconds to 1½ hours.^18,100

Emergence phase

During the emergence phase, uterine contractions cause the kitten to pass through the birth canal and pause in the vulva (Figure 6-5). Usually the amniotic sac has been broken by uterine contractions, but if not, the queen’s licking soon breaks it. The release of fluids from the amniotic sac causes the queen to spend additional time licking the fluids and coincidentally herself and the newborn.^43,53,100 Experienced queens may direct more attention to the newborn, but other behaviors are quite similar to those of the contraction phase.

Figure 6-5 The emergence of the kitten through the queen’s vulva.

Delivery phase

The third phase, delivery, represents passage of the fetus from the vulva¹⁰⁰ (Figure 6-6). Licking directed specifically at the newborn increases, although the queen may not begin immediately after the delivery. This licking supplies the stimulus for initiation of the newborn’s respiration if passage through the birth canal did not. A first-litter queen tends to be the most restless and is less likely to lick herself and each kitten correctly.²² Experience apparently is needed to refine these behaviors. From lateral recumbency the queen may try to reposition herself after the delivery and may coincidentally drag the kitten around by the still-attached umbilical cord, perhaps even stepping or sitting on it. Distress cries from this newborn or others are often ignored by the queen at this time, perhaps because of the excitement associated with parturition, or incomprehension of the vocal cue, or both.^22,100 Kittens can be injured during this period. Shortly after parturition, generally 1 to 4 minutes later, the female becomes responsive to the kittens.^18,100 She will sever the umbilical cord shortly after the delivery in about one third of the births (Figure 6-7).

Figure 6-6 The delivery of the neonate, still partially covered by the amniotic sac.

Figure 6-7 The queen severs the umbilical cord with her teeth.

There is tremendous variation in the intervals between kitten births, ranging normally from 32 seconds to more than 50 minutes.^53,100 Most kittens are born within 15 to 30 minutes of each other, with a total delivery time of 1 to 2 hours.^13,14 Some normal queens will take as much as 33 hours to complete the deliveries, but usually external disturbances, such as the absence of an owner or the moving of a nesting area, cause this extreme delay. Uterine inertia is relatively rare in cats.⁶¹ There is no relationship between the sequence of a kitten’s birth and the interval between its birth and that of its littermates.

Placental phase

The last of the four phases of parturition, as they usually occur, is the placental phase. During this time the placenta is expelled from the genital tract. Immediately before this expulsion, the female becomes restless, again appearing to focus her attention toward the caudal part of her body. She responds promptly to the emergence of this tissue, sometimes eating it before it has completely emerged¹⁰⁰ (Figure 6-8). No relationship has been shown between the sequence of the births and either the interval of response to the placentas or the rate and completeness of its consumption.¹⁰⁰ At times, a second or even third kitten is born before the umbilical cord of the first is severed or the placenta passed, but each will be attended to as time permits. Nutritive value from the afterbirth is considerable and allows the queen to spend more time with her offspring for the first few days than if she had to seek food as usual. In addition, this behavior minimizes the soiling of the nest area. The queen continues genital and neonatal licking during the placental phase but takes time to sever the umbilical cord with her carnassial teeth. Their crushing action, the stretching of the vessels, or both prevent fatal umbilical hemorrhage.^40,100 The queen’s care during this phase makes cannibalism as a consequence of overzealous eating of the placenta and cord very rare.

Figure 6-8 The queen responds to placental emergence by consuming the tissue.

For those queens sharing a communal nest, one may be assisted immediately postpartum by another female.¹⁹ The help usually is to clean and dry the young, but it can include severing the umbilical cord.²²