CHAPTER 28Stallion Reproductive Behavior
Evaluation of reproductive behavior is an integral part of the examination for breeding potential or problems in the stallion. An understanding of the sequence of behaviors displayed by the stallion in preparation for, during, and after mating is important for the diagnosis of disorders such as poor libido, erection, or ejaculation failure. Modern breeding practices do not allow display of the full array of stallion reproductive behavior. Therefore, knowledge of behavioral clues will be very useful in training the novice stallion for mating and implementing behavioral correction techniques.
NORMAL REPRODUCTIVE BEHAVIOR IN THE STALLION
Reproductive Behavior in Free-Ranging Stallions
Reproductive behavior of the stallion in feral or semiferal situation has been thoroughly described by several authors.1–7 In these conditions, breeding occurs in what is described as a harem social organization. A harem is composed of a mature stallion and a few mares and their offspring. In some situations, the main (primary) stallion in the harem may be “assisted” by a second stallion. The second stallion helps with defense of the group and will breed only on rare occasions (usually with young mares).5,7–12
The stallion tends his mares all year round. Reproductive status of the mares is continually monitored by elimination marking behavior (olfactory investigation of the mare or her urine or feces).13 Monitoring of the herd is increased during the peak of the foaling and breeding season. Stallions tend to spend more time closer to mature harem mares in estrus. The mare plays a primary role in initiation of reproductive behavior by soliciting the stallion, displaying strong estrous behavior signs, and allowing mounting.1–46,7
Precopulatory Behavior
Stallion display a characteristic precopulatory sequence beginning with nose-to-nose contact associated with a characteristic soft nicker vocalization. Oronasal investigation (sniffing, nibbling, nuzzling, and licking) follows, starting at the shoulder and elbows and proceeding to the ventral abdomen and udder and then to the hind legs and perineum.14 Flehmen response generally is displayed when the stallion comes into contact with urine or vaginal fluid.15,16 During this precopulatory behavior the stallion may nip the mare at the flank or hock. Rubbing or resting the chin on the rump may be displayed, as well as mounting without erection.
Copulatory Behavior
Copulatory behavior (mounting, insertion, thrusting, and ejaculation) may follow the precopulatory behavior immediately or may occur after several precopulatory sessions. The mare generally facilitates mounting and insertion, but the stallion needs a high degree of coordination and physical ability to complete this behavior.5 Insertion and organized thrusting occur over a period of 20 to 25 seconds before ejaculation is observed. Mares may move forward during copulation to accommodate the stallion, which also may serve to prevent injuries. Dismount occurs approximately 20 to 30 seconds after ejaculation.1
Erection and Ejaculation
Erection and ejaculation are controlled by nerves originating in the spinal cord. Erection occurs as a result of relaxation of smooth muscles of the corpus cavernosum and corpus spongiosum in combination with an increase in arterial blood flow to the penis.17 Penile rigidity is improved by contraction of the perineal striated muscles after engorgement and erection of the penis.18 The activity of the striated muscle is increased during copulation as a result of stimuli from the autonomic nerves to the corpus cavernosum and corpus spongiosum and from the somatic nerves to the ischiocavernosus and bulbospongiosus.19,20 Continuous stimulation by the vagina and pelvic thrusting further enhances this activity and promotes emission and ejaculation.
Emission occurs as a reflex to proper stimulation after 7 to 9 pelvic thrusts.21 During emission, the rhythmic contractions of the smooth muscle layer of the cauda epididymis, ductus deferens, and accessory sex glands serve to release spermatozoa and fluid into the urethra. Emission and bladder neck closure reflexes are primarily under α-adrenergic control involving preganglionic sympathetic fibers from the lumbosacral segment of the spinal cord and connecting with the caudal mesenteric plexus. Ejaculation occurs in 5 to 10 successive forceful jets produced by the rhythmic contractions of the ischiocavernosus, bulbospongiosus, and urethralis muscles, as well as sphincter muscles. Each ejaculatory jet is evident externally by a characteristic downward movement of the tail known as tail flagging. Ejaculation is controlled by the pudendal nerve and the sacral segment of the spinal cord.21–24
Masturbation
Spontaneous erection with penile movement and rubbing against the belly is described as masturbation in the male equine.25 Several studies and clinical observations have shown this to be a normal behavior.25 Masturbation occurs in all equids at regular intervals (every 90 minutes) and does not seem to be related to age, libido, fertility, or sociosexual conditions (e.g., type of housing, mare proximity).26–29 Masturbation behavior does not occur during standing or recumbent sleep but rather is seen during periods of quiet rest and may be elicited within a few minutes of return to calm after startle.25,30 Ejaculation during these periods of masturbation is extremely rare (less than 1 in 100 episodes); therefore, the common belief that semen “wastage” results from this behavior is not substantiated.25
Several devices—stallion rings, the brush, the basket, electrical collars—have been designed to inhibit or eliminate this behavior in show and performance horses. Clinical experience shows that these “anti-masturbation” devices are not effective and may even compromise stallion breeding ability.25 Recent reports show that aversive conditioning to eliminate masturbatory behavior by means of electrical shock suppresses sexual arousal and adversely affects breeding efficiency and semen quality.25 Stallions subjected to aversive conditioning showed an increase in erection latency, mount readiness latency, ejaculation latency, and mounts to ejaculation and a decrease in number of vocalizations, erection rigidity score, and ejaculatory pulses. Decreased ejaculation efficiency resulted in decreased sperm number in the ejaculate.25
Reproductive Behavior in Modern Breeding
Paddock or Pasture Mating
Introduction of a stallion to a group of mares or moving an established herd to a new unfamiliar surrounding results in increased snaking activity.31 This behavior, characterized by extension of the head and neck, holding the ears back, and lowering the head, usually subsides within a day or 2. New mares do not reinitiate snaking and herding behavior, but they may be kept at a distance by the stallion for up to 4 days.31,32 Stallion seem to adjust relatively quickly when moved from one paddock to another with different groups of mares.33 Although stallions in this system breed often (every 1 to 2 hours), pregnancy and foaling rates achieved in these systems generally are good if the stallion does not have any physical or genital problem.32,34,35 Unfortunately, this system is notorious for the increased incidence of stallion breeding injuries.36
In-Hand Mating
In general, the mare is teased by a different stallion and restrained in the breeding shed. The stallion is brought to the breeding shed using a halter or a breeding bridle. The contact time between the mare and the stallion is variable, depending on several factors. Typically, the stallion is directed to approach the mare from the hindquarters, skipping the major part of precopulatory sequence. Stallions in this system learn that their role is to walk into the breeding shed and perform breeding, so that the opportunity for precopulatory behavior is very limited. Most stallions will walk into the breeding shed already in erection and ready to mount, insert, and complete the mating with minimal sexual preparation. In some stud farms, it is not uncommon for the process of natural cover to involve more than six people, each of whom specializes in a small detail of mare and stallion preparation and handling. This is hardly a natural breeding environment, and interpretation of stallion reaction should be done very carefully.
Mount without erection is not as frequently seen in this situation as with free-ranging horses, probably as a result of “specialization” of the stallion or repression of the handler.37 In one study of experienced stud farm stallions, mounts without erection were observed in only 6 of 85 attempts.37 In my experience, mount without erection is observed more frequently in young novice males and during the second ejaculation. Mount without erection is rarely observed during the breeding season in stallions that are used with moderate frequency for breeding. Although mounting without erection is a normal behavior, some stallion handlers may reprimand stallions, thereby conditioning them not to mount until they have achieved full erection. It is not known whether mounting without erection (false mount) results in improved seminal characteristics in terms of sperm concentration and volume.
The time from introduction to the breeding shed to erection (erection latency) ranges from 10 to 163 seconds.14,37,38 Variations observed in this latency may be due to differences in management procedures and in stimulation provided. In one study, no significant correlation was found between age of the stallion and erection latency.37
Ejaculation latency varies depending on the individual stallion and the frequency of mating. In a study conducted on French stud farms, a majority of first mounts (75%) resulted in ejaculation.37 In another report, ejaculation occurred after 1.8 mounts.39 The number of mounts per ejaculation generally is higher out of season than during the breeding season.37,39 Ejaculation latency increases between the first and the second mounts.37
Semen Collection
Semen collection for the purpose of reproductive evaluation or for use in artificial insemination is widely practiced in modern horse breeding. Although semen collection can be performed on jump mares, the standard accepted method is to train the stallion to mount a phantom, or dummy. Stallions can be readily trained to serve the artificial vagina. Stallions trained to perform in these conditions do not necessarily lose their ability to breed naturally. Semen collection using a phantom, however, is characterized by a complete absence of auditory, olfactory, and vaginal contact and contraction stimuli. It is well established that these stimuli reinforce erection and ejaculation in the stallion.40 Some studies have reported that more mounts are necessary per ejaculation for semen collection than in natural cover.39 In a recent study comparing behavior during natural cover and semen collection on a phantom in 42 stallions, however, no statistically significant difference was found in erection latency (62 ± 22 seconds for natural service versus 100 ± 13 seconds for phantom collection) and ejaculation latency (84 ± 18 seconds versus 86 ± 28 seconds, respectively).37 These findings suggest that appropriate training and adjustment of artificial vagina conditions (temperature, pressure, and position) are important and should be adjusted for each stallion to allow a repeatable technique for adequate semen collection.41,42
In my experience, training of a novice stallion to semen collection using an artificial vagina and an estrous mare is successful in more than 90% of instances after one or two attempts. Training for semen collection on a phantom may take a little longer. Steps for training stallions for semen collection on dummies have been thoroughly described. The key points in this technique are to use an estrous mare for stimulation of the stallion and to allow a few mounts on the mare, alongside the phantom, before attempting in a later session to divert the stallion’s mounting efforts to the phantom.43 Presence of an estrous mare is not necessary after initial training.37 Semen collection on a phantom or on the ground (i.e., standing collection) does not affect natural cover, and vice versa.37,44
NORMAL REPRODUCTIVE BEHAVIOR IN JACKS
Male donkeys (Equus asinus) are described as territorial.45–47 Each jack has a territory in which breeding of solitary females takes places.46 Jacks defend their territory against any adult males, particularly in the presence of estrous jennies. The jack typically interacts with jennies in a series of brief episodes, interrupted by a retreat to his resting area. The precopulatory sequence includes vocalization within the resting area; approach to and teasing of an individual jenny, followed by a retreat; and then a sudden approach with brief teasing or mounting. This sequence may be repeated several times before the jack retreats again to the resting place, where erection is achieved before he immediately approaches a jenny and copulates quickly without precopulatory behavior.47 Specific precopulatory behaviors include nasonasal contact; nibbling or sniffing of the head, neck, back of the knee, body, flank, perineum, and tail; olfactory investigation of voided urine or feces; and flehmen.47,48 Achieving an erection at a distance from jennies is one important characteristic of breeding behavior in the jack. Spontaneous erection and masturbation occur at the same rate as in the horse, with an episode every 90 minutes on average.28
Insertion latency, number of thrusts, and total time mounted for free-ranging donkeys have been described as similar to those for horses.35 However, in hand-mating situations and, in particular, in situations of mule production (jacks breeding mares), my experience has been that all jacks take an extremely long time to erection and mount, but that once mount is achieved, ejaculation generally is easily obtained.49
Hand Breeding in Donkeys
Breeding Donkeys to Jennies
Space for and freedom of interaction between the jack and the jenny seem to be key factors in sexual stimulation. The time to first mount increases if the jenny is restrained.47,50 It is recommended that enough space be provided during in-hand mating of a jenny for the jack’s retreating behavior to take place. The slow/fast retreat from the female is a unique behavior in jacks.48,51 The number of retreats generally is higher for the first ejaculation than for successive ejaculations.50 Presence of other receptive jennies may enhance sexual stimulation, whereas presence of other jacks may distract or inhibit sexual activity, in keeping with the territorial nature of this species.52 The time from introduction to a female to mounting and ejaculation varies, ranging from 6 to 32 minutes in various studies.47,50,52,53
During the precopulatory and copulatory phases, jacks exhibit a sequence of behaviors including nasonasal contact, flehmen responses, mounting without erection, partial and total exposure of the penis, sniffing and biting specific areas of the female body, lip clapping, and slow/quick retreats with vocalization.51–53 These behaviors show significant individual variation.50
The frequency of flehmen response (5 to 8) is generally higher than in stallions47,50,51 and does not seem to be affected by rank of ejaculation.50 The initial reaction of the jack in the breeding shed is vocalization, which is followed by one or several mounts without erection. The first mount is performed without erection in 70% of the cases.47,50,52,53 The number of mounts without erection varies from one study to another and probably is affected by training and handling differences.47,48,50
Frequent partial exposure of the penis during the precopulatory phase is common in jacks.47,48,52 Total exposure of the penis generally is followed by erection.50 The first erection does not always result in ejaculation. Jacks may show several erections and masturbation before mounting and ejaculation.47,48 The mean time from first contact with the female until the first erection varies, ranging between 10 and 15 minutes.50 Depending on the individual animal, from 4 to 8 pelvic copulatory movements occur before ejaculation.47,48,50 A seasonal effect on libido has been reported by some authors, with decreased latency to first mount, first erection, and ejaculation during spring and summer (breeding season).52 This seasonal effect may vary from one geographic region to another.50
Breeding Donkeys to Mares
In my experience, breeding jacks to mares is more challenging, with often increased latency to erection, mount, and ejaculation. In pasture breeding systems, lack of conditioning of jacks to breed mares may result in lower reproductive efficiency. It has been suggested that jacks destined for mule production should be raised with horse fillies after weaning and prevented from any contact with jennies until they are adult.48,54
In pasture, precopulatory, copulatory, and postcopulatory behavior for jacks breeding mares are similar to those for jacks breeding jennies.51 The interaction between mares and jacks is reportedly shorter in duration but more frequent. Also, mares do not display behavioral estrus with the same intensity to jacks as they do toward horse stallions. In one study, the percentage of estrous mares exhibiting signs toward a jack ranged between 28% and 43%, whereas 93% exhibited sexual behavior toward stallions.51,54 In a stud farm situation, I have observed latency to erection and ejaculation of up to 120 minutes when stallions are bred to hobbled estrous mares.49 In addition to these behavioral differences that may affect fertility results, size discrepancy may be another constraint in jack-mare breeding.
ABNORMAL REPRODUCTIVE BEHAVIOR
Sexual behavior dysfunction has long been recognized as an important cause of equine reproduction failure.55–59 A variety of behavioral problems have been identified, including low sexual arousal, preferences for certain mares, preference for handler or handling conditions, aggressiveness toward the mare or handler, self-mutilation, abnormal copulatory behavior, failure of erection or ejaculation, and unruly behavior during mating.14,43,56,57,60–63
Despite this inventory of behavioral problems occurring in stallions, very few detailed studies on the prevalence of specific problems in the stallion population have been performed. In addition, most relevant reports are restricted to clinical observations and therapeutic trials based on a limited number of cases.14 Several disorders manifesting as behavioral problems are secondary to a specific physical difficulty or endocrine disturbance. Therefore, diagnosis of the cause of what is perceived as a breeding-related behavioral problem requires a multidisciplinary approach involving an orthopedic specialist, a theriogenologist, and a behavioral specialist. A thorough medical and breeding history should be taken, including previous injuries during breeding, handling routine, changes in handling, and time of onset of the problem.
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