The onset of puberty and reproductive activity during a filly’s first ovulatory cycle is affected by her season of birth. Spring-born fillies tend to ovulate during the late spring when they are 12–15 months old, whereas late-born fillies show surges of luteinizing hormone (LH) and progesterone that allow some (but not all) of them to display estrus and ovulate at younger ages.¹ When planes of nutrition are marginal, such as in the free-ranging state, puberty may not occur until the filly’s third spring.² Although fillies show a characteristic seasonal pattern of plasma follicle-stimulating hormone (FSH) and LH fluctuations even when ovariectomized, probably as a result of secretions by the adrenal cortex,³ their breeding season appears to be shorter than that of adult mares.¹ In their free-ranging state, fillies usually seek contact with bachelor stallions or with unfamiliar harem stallions. When seeking sexual activity with resident, and therefore familiar harem stallions, fillies are likely to be ignored, especially if more mature mares are concurrently receptive. This allows subordinate stallions to consort with these young females and perform so-called ‘sneak matings’ (which are associated with low conception rates).

In terms of their social integration with other horses, mares can be categorized as being loyal to a single stallion, part of a multi-stallion band or social dispersers (females in transit – so-called mavericks).⁴ Interestingly, compared with the mares in single-stallion bands, the disperser mares have been shown to have a greater parasite burden and poorer body condition despite spending a similar amount of time feeding.⁴ Compared with all other mares, they also have the lowest fecundity and the greatest offspring mortality rates. A mare is thus much more likely to pass on her genes if she retains the companionship of at least one stallion. Beyond that, the stability of the mare–stallion relationship in single-stallion bands, with its resultant containment of agonistic behavior, contributes considerably to reproductive success and therefore biological fitness.^4,5

Mares will regularly interfere with other mares during courtship and mating. The behavior of a mare in response to seeing another mare having contact with her stallion depends on her rank and reproductive state, being most obstructive when she is in estrus.⁶

In general, mares become increasingly receptive towards stallions as they age and will continue to breed until their early twenties.⁷

Being seasonally polyestrus, mares show a cyclical active estrus⁸ (7.1 ± 4.2 days) and quiescent diestrus⁸ (16.3 ± 2.9 days) throughout the breeding season⁸ (152 ± 50 days). Season lengths become more restricted as one travels nearer the Poles.⁷ Of all ungulates, horses have highly variable cycle lengths⁹ and for this reason variations in estrous cycle are completely unreliable as a means of diagnosing ovarian dysfunction. Cycles, of which there are a mean of 7.2 ± 2.0 per year,⁸ vary in length and behavior, with some mares showing a shift in temperament from normally placid disposition to irritability and vice versa. More common in fillies than in mares, protracted estrous periods of up to 50 days have been reported,¹⁰ while their contraction as a result of veterinary examinations per rectum has also been noted.¹¹

The duration of estrus decreases at the height of the breeding season (Fig. 12.1), the trend being matched by reciprocal increases in diestrus duration that keep the length of the whole cycle relatively constant.

Figure 12.1 Variation of estrus and diestrus duration during the northern hemisphere breeding season.

(After Ginther.⁸ Redrawn, with permission, from Waring.²)

Mares reject advances by stallions and show relative disinterest in their company during diestrus and during periods of rising and high plasma progesterone concentrations.¹² A diestrous mare approached by a stallion becomes restless, switching her tail and flattening her ears as she threatens to kick, strike or bite (Fig. 12.2). Because behavioral responses associated with estrus may persist to varying extents in mares in anestrus,^13,14 it is important for stud personnel to take repeated measures of responses to teasing so that changes in frequency of responses, rather than the presence or absence of responses, can be monitored.

Figure 12.2 Illustration of the ways in which the mare’s behavior changes throughout the estrous cycle. FSH, follicle-stimulating hormone; LH, luteinizing hormone; PROG, progesterone; EST, estrogen; PROST, prostaglandin.

(After Noakes DE et al, eds; Arthur’s veterinary reproduction and obstetrics; London: WB Saunders; 2001.)

Even when a mare is receptive, squealing and strike threats may occur as a preliminary part of the nasal contact phase of a successful sexual encounter. Estrus in the mare is characterized by courtship behaviors such as abrupt halts during locomotion, approaching and following stallions, lifting the tail (before being mounted or after being mounted), clitoral winking (Fig. 12.3) especially during teasing, urinating (up to 21 urinations in an hour have been recorded¹⁵), and tolerance of the stallion’s pre-copulatory behavior such as sniffing and nibbling. Depending to some extent on individual differences between mares, receptivity peaks 1–3 days prior to ovulation (although this has been disputed¹⁶). Above all, estrus in the mare is defined by her standing firmly with her tail up while being mounted.¹³ Ovulation typically occurs 36 hours before the end of estrus and is marked by the decline in the mare’s receptivity.

Figure 12.3 Clitoral winking in an estrous mare.

Estrous mares frequently follow and place themselves in the vicinity of a stallion, especially if contact with him is intermittent.^6,17 If their solicitations are ignored, mares may display the estrous stance nearby periodically or, if this fails to attract the attentions of the harem stallion, they may even disperse in search of other males. Occasional mares exhibit signs of colic during estrus to the extent that they are presented for bilateral ovariectomy.^18,19 There are also occasional instances of estrous mares mounting or being mounted by other mares.² Strangely, in Icelandic mares, this response is regarded as normal even when a stallion is present and is used by stud managers as an indication of early estrus. The estrous mares are almost always mounted, while the mounting is most usually performed by pregnant mares (Machteld van Dierendonck, personal communication 2002).

While prolonged tail-raising, the urination-like stance and clitoral winking in combination with the increased vascularity of the vaginal mucosae seem to provide strong visual attractants for stallions, facial expressions in estrous mares have also been noted. Open mouths and bared teeth are common in the females of wild asses that adopt forced mating styles. Called ‘Rossigkeitsgesicht’ in zebras (Fig. 12.4), this accompanies the characteristic urination stance to contribute to the composite attractive signal to stallions.²⁰ The response is also seen in occasional mares,²¹ with Standardbreds more likely to demonstrate it than Arabians.²² Likened to the snapping response of juveniles in the presence of a threat, this response is interpreted by some observers as a sign of submission² or conflict²¹ while others have demonstrated that it can elicit aggression from observing horses.²³

Figure 12.4 Drawing of two successive stages in the threatening Rossigkeitsgesicht response of a Grant’s zebra (E. burchelli boehmi).

(Redrawn from Waring GH, Wiersbowski S, Hafez EFE; The behaviour of horses; In: Hafez EFE, ed; Behaviour of domestic animals; 3rd edn; London: Baillière Tindall; 1975.)

Although pony mares have been described anecdotally as having more distinct ovulatory and anovulatory behaviors,² other data suggest that cold-blooded mares are more likely to have silent estrus than other breeds.²⁴ Meanwhile, reduced antagonism to teasing when not in estrus and generally subdued manifestations of estrus are also reported in association with compromised thyroid function.²⁵ The average interval between the first signs of estrus and ovulation is 5.16 ± 2.65 days.²⁶

Although they are irregular, estrous cycles are common in mules and the extent to which these hybrids are functionally infertile varies considerably.²⁷ Mules often have follicles that ovulate and luteinize but they generally lack oocytes (Lee Morris, personal communication 2002). That said, they do very occasionally bear live foals.²⁸

The importance of auditory perception in eliciting typical estrous responses has been highlighted by studies of the relative effects on mares of audio recordings of the characteristic stallion nicker versus the presence of a stallion.²⁹ In response to these recordings, estrous mares, especially barren ones, showed overt estrous behavior including tail-raising, clitoral winking and abduction of the hindlegs. Maidens and mares with foals at foot exhibited some of these reactions but at a lower frequency. There are reports of reasonable efficiency in detecting estrus in mares by playing back recordings of stallion vocalization with and without added stallion scent. That said, for this to be a useful part of stud management in the absence of a stallion or teaser, a minimal schedule of three times weekly would be required. In a four-week study of 11 mares estrus was detected with the stallion auditory and olfactory stimuli method, on average more than four days before 80% of ovulations.³⁰ Although the usefulness of stallion vocalization recordings used in isolation in estrus detection has been contested,³¹ when used in combination with palpation of the inguinal region of mares this approach was reported to be 97% accurate.³²

The length of courtship a mare receives from a harem stallion depends on her rank. A high-ranking mare may be courted for several days before a series of matings takes place. Only then does she tolerate the stallion attending to other mares in the group.

During copulation the mare adopts a characteristic base-wide stance that helps her to balance. Although her neck is usually lowered, she remains very alert with her ears upright. She may look round slightly to monitor the stallion, especially during ejaculation.¹⁵ Dismounting is often assisted by the mare moving forward.³² The couple remain reasonably close to one another after copulation and the mare continues to raise her tail and urinate until grazing and social interactions with others take priority.³³ In the free-ranging state, matings will occur approximately six times per heat in single-stallion groups.³⁴ It is important that we recognize the many ways in which hand-breeding can so easily compromise a mare’s ability to behave normally during courtship and copulation (Fig. 12.5).

Figure 12.5 Restraint in the hand-bred mare often involves the use of a twitch and service hobbles, which may alter her locomotory behavior and ability to signal. Meanwhile, her appearance may be further affected by the use of a breeding cape to prevent her from being damaged by the stallion’s teeth as they are used to grasp her neck, and by the use of tail wraps. It is not clear how much these interventions influence the mare’s physiological stress response and the stallion’s performance.

Hormonal control of ovulation can be achieved by using exogenous steroids with or without prostaglandins.⁵⁰ Estrous displays can be induced by administering exogenous steroids.⁵⁰ For example, estradiol elicits soliciting behavior within 4 hours of injection, while progesterone usually results in the absence of sexual behavior.^3,51 Altrenogest can be given orally to regulate estrous behavior early in the year, and its withdrawal will synchronize estrus in cycling mares and those previously exposed to artificial light.⁵² Conversely it has been suggested that endometrial edema as appreciated by ultrasonography may indicate the optimal time for coitus and provide an instant indication that the basal concentration of progesterone is <1 mg/mL.⁵³ But estrus is not purely a product of hormonal flux, since estrous behavior reflects a combination of other factors, including the presence of a stallion, social rank and duration of teasing. For example, when mares are stimulated by restrained teasers, their estrous display lengthens.⁹ Similarly, failure of estrus can often be due to the absence of exogenous factors such as odors, sounds, sight and touch⁹, e.g. that arise with appropriate attention from stallions.

The gestation period of the mare is approximately 11 months or 340 days, with generally slightly shorter periods in smaller breeds.⁵⁴ Gestation duration in a large study of Australian Thoroughbreds⁵⁵ (n = 522) ranged from 315 to 387 days (mean 342.3 days). The survival rate of Thoroughbred foals delivered at less than 320 days of gestation is approximately 5%.⁵⁶

Factors that influence the duration of a mare’s gestation include her plane of nutrition towards the end of her pregnancy and the sex of the foal. Howell & Rollins⁵⁷ found that mares on higher planes of nutrition tend to foal earlier than those on maintenance diets. In the free-ranging state, mares normally foal in mid to late spring, a strategy that usually ensures sufficient feed being available for lactation. By showing that foals conceived in early spring had longer gestations than those conceived in mid to late spring, Hintz et al⁵⁸ confirmed the importance of seasonal effects on the biological fitness of foals (a similar trend was reported by Campitelli et al⁵⁹). The sex of the foal contributes to the duration of gestation, in that fillies are generally born 1–2 days before colts.⁵⁵ Mares lose more condition prenatally when carrying a colt if they were originally in good condition at the time of conception, but more when carrying a filly if they were in poor condition.⁶⁰

While some mares become actively aggressive to approaching stallions during pregnancy, others may remain friendly⁶¹ and raise the suspicion that they are returning to estrus. After between 40 and 70 days of pregnancy, follicles are produced in response to eCG.⁶² They are generally large in size and remain active, ovulating to form accessory corpora lutea. Estrogen produced from these follicles is thought to prompt some pregnant mares to consort with stallions and exhibit some estrous behavior during the first trimester of pregnancy. The response occurs more frequently in mares bearing female foals than in those bearing males.⁶³ Up to 35% of ovariectomized mares,¹⁸ and also mares in an anovulatory period, show sexual responsiveness.^1,3 This suggests that mares’ ability to dissociate sexual behavior from ovulation may persist even when they are pregnant. However, these manifestations (which may occur a mean 1.76 times per pregnancy³⁹) often lack the usual potency associated with ovulation. Asa¹⁷ suggests that non-reproductive sex may serve to influence stallions to remain with their bands during the non-breeding season.

Asa et al⁶² examined the effect of adding a stallion to an established group of 12 pregnant pony mares. After the experimental introduction of stallions into random harem groups, full estrous behavior was not observed. Instead, only weak signs of estrus were noted, with only four mountings recorded and only a single tail raised. Social interactions such as grooming between the mares increased, while the only approach between mares and the stallion was an initial ritual greeting early on in each exposure.

Although the behavior of the mare does not change markedly in the months leading to parturition, significant differences arise immediately before foaling.^2,62 Shaw et al⁶⁴ examined mare behavior 2 weeks prior to parturition. A total of 52 pregnant mares in box stalls were observed at 30-minute intervals between 1800 hours and 0600 hours. In the 2 weeks before foaling, mares spent 66.8% of their time standing, 27% eating, 4.9% lying in sternal recumbency, 1% lying in lateral recumbency and only 0.3% walking. Challenging the notion that the mare reduces her ingestive activities immediately prior to parturition,^9,61 eating was the only behavior unaffected by the imminent foaling. On the night of foaling, mares spent less time standing (53.3%) and more time in sternal (8%) and lateral (5.3%) recumbency and walking (5.3%).⁶⁴ This reflects the restlessness of mares when they are about to foal and the fact that they almost always choose to foal in a recumbent position (a characteristic that led to the development of foaling belts that can detect recumbency).

In their free-ranging state, mares about to foal often become parted from the herd either by seeking relative isolation (sometimes accompanied by older offspring or another adult mare) or by being left behind. Along with the other peri-parturient behaviors, this strategy provides a nurturing environment for the foal and helps to avoid mis-mothering, in accordance with the ‘binding theory’ offered by Klingel.⁶⁵ Average time spent walking tends to increase on the day of birth (most notably the 30 minutes prior to parturition), with higher-ranking mares tending to try to separate themselves furthest from the herd, and maiden mares remaining reasonably close.^66,67 Mares confined in a box stall, on the other hand, may be required to foal within auditory, olfactory and visual contact of other mares. They are often described as being alert, uneasy and restless before parturition.⁹ This may be due, at least in part, to their motivation to separate themselves by locomotion being thwarted. While physiological changes include swollen teats, distended udder and softening of the cervix, behavior changes may also include swinging and rubbing the tail against fixed objects as the vulva becomes relatively flaccid.⁶¹

It seems that regardless of the bond they may have with particular personnel, most mares prefer not to foal in the presence of humans and, perhaps in a bid to ensure isolation, may delay foaling by prolonging the initial stage of parturition.^2,64 When left undisturbed, most mares foal at night (e.g. in Shaw et al’s study⁶⁴ 86% foaled between 1800 and 0600 hours), presumably as a means of avoiding daytime predators. Fraser⁹ proposes that colts are born later in the night than fillies and rather unconvincingly suggests that this is for the ‘good of the species’ since fewer males are required for reproductive success of a group. There is evidence that the percentage of night births is higher in spring than in winter⁵⁹ although others report that seasonal daylength and onset of darkness have no effect on the mean time of foaling.⁶⁸

Continual disturbance, especially at night may adversely delay the onset of foaling.⁶⁸ On many studs, laudable attempts to minimize human interference and reduce imposing unnatural delays include using one-way mirrors and video surveillance equipment. However, the avoidance response seen in most mares during foaling is by no means universal. Some mares even appear to seek human company at this time.⁶¹ It would be interesting to see how attempts to ‘imprint’ fillies (see Ch. 4) affect their responses to humans when peri-parturient.

Immediately prior to parturition the mare’s behavior increasingly involves stretching, yawning, repeated recumbency and standing, walking, tail-swishing, kicking, looking at flanks, pawing at the ground, crouching, straddling and kneeling. These responses all imply that she is undergoing abdominal discomfort⁹ that may last from a few minutes to hours.² Patchy sweating on the flanks and girth area indicates that first-stage labor is about to commence. This and persistent raising of the tail seen at this stage gave rise to the emergence of parturition detectors (e.g. as described by Bueno et al⁶⁹).

Depending on their force and timing, contractions induce different responses in the mare.⁶¹ With modest contractions she may swish her tail or stamp a hindleg. Larger, more powerful contractions cause her to become transiently tucked up in the flank or to lift her tail over her back and lean backwards onto her hindlegs.

Usually, when the placenta ruptures and the allantoic fluid escapes, indicating the second stage of parturition, the mare lies down (a response often accompanied by the greatest passage of fluid) in preparation for forceful and repeated straining. Some mares may investigate the fluid and consequently exhibit flehmen and occasionally nicker.¹⁰ Sternal recumbency is commonly adopted but it is not unusual for the mare to stand and reposition herself repeatedly, especially if she is disturbed.⁷⁰ Vigorous rolling is also reasonably common and is thought to represent attempts to correctly position the foal. The foal’s forelegs either side of or to one side of its head engage in the vagina, then may emerge from the vulva covered by a veil of amniotic membrane (Fig. 12.6).

Figure 12.6 Foaling sequence.

(Photography by Neil McLeod.)

Straining efforts, numbering between 60 and 100 (n = 5), are required especially to expel the foal’s forequarters and head.⁷⁰ Data from Thoroughbreds suggest that compared with experienced brood mares, maidens spend slightly longer in second-stage labor (mean of 21 minutes for primiparae versus the mean of 18 for experienced mares⁷¹), while pony mares take an average of 12 minutes.⁷² Foals from primiparous mares are considered to be at high risk of thoracic trauma.⁷³ The final expulsion is usually achieved with the mare in lateral recumbency with legs extended. Expulsive efforts may cause the mare’s upper hindlimb to become raised. With the emergence of the foal’s head, forelimbs and hips, the second stage of parturition is complete. Unless disturbed, the mare then usually remains in lateral recumbency, often with the foal’s hindlimbs still in the vagina.

The third and final stage of parturition involves the transfusion of blood from the placenta to the foal during the post-partum pause and the passage of the placenta.⁹ If parturition occurs without difficulty then, after the post-partum pause which allows blood to leave the placenta and reach the foal,⁷⁴ the foal will free itself of fetal membranes by raising its head and will sever the umbilical cord as it moves away from the mare.

Third-stage labor is marked by signs of abdominal discomfort, including looking at the flanks, sweating and pawing – behaviors that seem to have a stimulating effect on many observing neonates. Approximately 1 hour after delivery of the foal, the placenta is expelled, often as the mare rises from a bout of rolling. Mares typically show some olfactory investigation of the membranes, which elicit flehmen responses and occasionally some perfunctory nibbling. In the free-ranging state, the mare and foal leave the site of foaling soon after the placenta is discharged. This is thought to contribute to biological fitness by avoiding predators that may be attracted by the odors of the fluids and membranes passed during parturition. It also marks the mare’s return to the relative safety of her herd, which may be seen moving towards the fresh dyad to investigate. High-ranking mares have been observed to take longer to rejoin their affiliates than subordinates.⁶⁶