Mating Behavior and Ejaculation

Rutting behavior in the dromedary

The onset of the breeding season is characterized by the display of a series of behavioral changes called “rut"’.^{(3, 49, 111)}

Aggressiveness

The onset of the breeding season is accompanied by an increased aggressiveness of the male dromedary toward other animals in the herd (especially other males) and sometimes even toward people. They become easily excitable and very hard to handle. Confined males show increased pacing and anxiety, and attempts to break out of the corral or pen are very frequent. During this stage, they can inflict serious wounds by biting strangers or other males. In fact, biting is the most common serious accident in handling breeding camels^{(11, 82, 111)} (Anouassi and Tibary, personal observations). During the breeding season, male dromedaries spend most of their time guarding the herd and surveying it for the presence of receptive females or an approach by strange males. Because of this continuous stress, a net reduction of food intake, and increased digestive transit (frequent diarrhea), all males tend to lose weight (up to 35%), sometimes to the point of emaciation (Figure 2.5). Aggressive behavior during the breeding season is also described in the Bactrian camel.⁽²⁷⁾ In a free-roaming herd, dominant males chase each other and engage in fighting which can lead to serious injuries.

Soft palate ejection and vocalization

Sexual behavior in the camel is also characterized by exteriorization of the soft palate (cf. Anatomy). The protrusion of this structure occurs all day long at an interval of 15 to 30 minutes and is accompanied by a loud gurgling/roaring sound. Protrusion of the soft palate becomes more frequent with increased excitation (presence of another male or passage of females).^{(49, 50, 56, 82, 87, 111)} Some dromedaries do not exhibit complete exteriorization of the soft palate, only a mere flapping; these are usually older animals or animals that have had their soft palate removed surgically during their racing careers. The soft palate is generally ejected from the right side but it can occur on the left side also. The reason for this side predisposition is not clear.^{(20, 21, 49, 50, 56, 87)}

The male also frequently produces a metallic sound by grinding the molars with lateral movements of the lower jaw. This sound can be produced any time but usually replaces the gurgling and soft palate ejection during copulation. A great deal of frothing is also evident during the breeding season. It is generally attributed to increased secretion of the salivary glands and the frequent exteriorization of the soft palate (Figure 2.6).^{(49, 50, 56, 87)} Frothing is sometimes so profuse that the head of the female becomes covered by blobs of saliva during mating. Frothing is also observed in the Bactrian camel (Figure 2.6).

Marking

Marking is one of the main sexual behaviors exhibited during the rutting season. It usually takes two major forms: 1) urine spraying and 2) poll-gland secretions smudging. The former behavior is exacerbated in the presence of another male, when females are passing by, or when the male is introduced into a new female herd.

During the spraying activity, the dromedary has a peculiar posture (Figure 2.7). The male assumes the crouched urination posture, while his hind quarter is flexed slightly with legs widely spread. Urine is ejected towards the back in small quantities and spread over the croup of the animal and surrounding areas with regular tail flogging (upward/downward movements of the tail) (Figure 2.7). The tail is held between the legs under the preputial opening for a few seconds and soaked with a stream of urine which then is sprayed by 4 to 5 beats of the tail. This series of spraying is repeated frequently (3 to 5 times per hour) during the day, so that a few weeks after the beginning of the breeding season, the skin over the sacral region becomes dark and thickened due to formation of a crust of mixed urine and sand (Figure 2.7).^{(56, 89)} The exacerbation of urine spraying in the presence of other males is usually accompanied by an increased frequency of gurgling, soft-palate exteriorization and teeth grinding. Urine spraying is also observed in the Bactrian camel (Figure 2.6).

The second type of marking behavior is used to disseminate the characteristic secretion of the poll gland. During the breeding season, the secretion of the poll glands is very copious. It is light brown or amber when first excreted but becomes tarry and dark - sometimes almost black - after a few minutes. It can be easily seen dribbling down the neck of the active male and has a very strong, fetid smell (cf. Anatomy). The area corresponding to the poll glands becomes large and darkened due to the increased activity.^{(49, 50, 56, 82,  87)} These secretions probably contain, in addition to androgen, some type of pheromones that are used to mark a territory. The rutting dromedary displays a frequent rolling and rubbing activity of the neck on small bushes or on the sand, especially when introduced into a new environment. This activity is most likely designed to smudge the secretion of the poll glands (Figures 2.8). Both types of marking behavior (urine spraying and rolling) have been described in the Bactrian camel.⁽²⁷⁾
 

Female seeking

During the breeding season, male dromedaries will continuously seek receptive females. They sniff the Hank and perineum of females and frequently display a flehmen (Figure 2.9).^{(63, 81, 111)} Males which are running free in the herd, will frequently chase individual females and force them down for breeding. This could also be an important factor in the weight loss of the male dromedary observed during the breeding season. Khan and Kohli⁽⁵⁰⁾ reported that such males can go without food and water for up to 3 weeks and spend most of their time encircling the herd and defending it against other males.

Rutting behavior in the South American camelids

Alpaca males exhibit different sexual behavior patterns if they are maintained with females all year round than if they are run in separate flocks. In the former case, they show distinct seasonal variations in activity while in the latter they show continuous libido and breeding capability, serving females whenever the opportunity arises.⁽³⁷⁾ Higher plasma testosterone levels have been found in the latter situation⁽⁶⁰⁾ but no related changes in fertility rate have been reported.⁽¹⁰⁵⁾ Aggressive behavior toward other males has been observed culminating in a direct confrontation with biting, necking and chest ramming that can lead to serious injuries, especially if the canine teeth are well developed.^{(19, 39)}

Mating behavior

Copulation is completed with the female sitting in the sternal position in all camelidae species (Figure 2.10). The male, squatting with his hind limbs completely flexed, sits on the ground using the surface of his heels and hocks. The fore limbs are extended on each side of the female with the feet rarely reaching the ground. The duration of copulation is very variable (Table 2). Amongst factors affecting the length of copulation are breed, age, sire, season, and frequency of use. Duration of copulation tends to be shorter at the beginning of the season and in younger males. The copulation time decreases as weather becomes warmer and the end of the breeding season approaches (Figure 2.1 I and 2.12).⁽⁷⁸⁾

The Bactrian camel exhibits the same copulation behavior. According to one study, copulation time is limited to 1 to 6 minutes in 86% of the matings but can be as long as 10 minutes.^{(26, 27)}

Duration of copulation in alpacas is affected by the age of females and by the presence of other males. Length of copulation is longer for multiparous females (21.5 minutes) than for maiden females (14.7 min.). Also, when several males are present in the same herd, copulation will be less than when no other males are present (8 vs. 21.5 min)^{(19, 91, 93, 94)}

Free mating

In a free mating system, male dromedaries will chase the females and force them to sit. A bull camel is usually allowed about 40-50 females in a season, but he generally remains in the herd all year round.⁽⁸²⁾

All South American camelids display flehmen behavior after smelling fresh female dung. They lift the head, elevate the upper lip without curling it, and open the month slightly.^{(19, 39, 40)} Contrary to what is observed in the dromedary and the Bactrian camel, South American camelids do not sniff the perineal area.

When introduced into a herd the male will chase a receptive female and try to force her down by mounting and putting pressure on the pelvis. This is contrary to the large camelids which will force the female to sit by putting pressure on the neck (Figure 2.13) probably because of the difference in agility and size. Erection is only achieved after the female is mounted in a sitting position. The perineal area is probed by the partially extended penis to localize the opening of the vulva. The penis is not fully extended until after intromission is complete. At this point the male moves his pelvis close to the pelvis of the female and effectuates short pelvic thrusts. As with the large camelid, the activity of the penis is accompanied by a rotational movement (corkscrew) of the glans penis.

In the llama, copulation lasts 5 to 50 minutes, but there is no correlation between copulation time and conception rate.⁽⁴⁰⁾ The male will attempt to breed the same female again on the same day or a day later unless she ovulates in which case she will "spit off". Similar observations have been made in alpacas. Vigorous male llamas can breed up to 18 females in one day for the first 4 to 5 days after introduction into a group of non-mated females. This decreases sharply after the first 2 weeks when the males lose interest even in females that are returning to estrus. Seventy percent of the breeding takes place in these first days with a conception rate of 50%.^{(91, 94)} It is generally recommended to change males every two weeks so that all females can be bred during a short interval of time. In alpacas, aggressive behavior toward other males and sometimes females has also been reported (biting neck, scrotum, ears).^{(91, 94)}

Hand mating

Fland mating is the breeding method of choice in several countries where there is a high demand for a particular stud (as is the case for racing dromedaries). This breeding method has several advantages such as a reduction of the risk of injuries by limiting the male's interaction with the female, precise breeding records, guided intromission limiting the risks of anal breeding or introduction of sand into the vagina and the uterus. In the case of hand mating, the female is introduced into the male's pen. The period of courtship is usually very short especially if the male is used to this kind of management of breeding. Sniffing of the perineal region and display of flehmen is observed after which the male tries to force down the female. Most receptive females will sit down immediately and assume breeding position. Identification of receptive females is, however, difficult in this type of breeding management and many docile females can sit without really being in the right stage of the cycle. In several instances we have observed that a male will breed non-estrous and even pregnant females. One interesting observation made at our laboratory was that all males readily accepted bilaterally ovariectomized females. Contrarily, several females that were diagnosed as receptive on the basis of ultrasonography and palpation were not readily accepted by some males. Females that are not accepted by a male will usually be bred by a different male. Similar observations concerning breeding non-estrous females or refusing estrous females were also made for llamas.^{(39, 40)} The reason for this behavior is not known. During mating, some males can stand for a long moment "guarding" the female before deciding to crouch and breed. This is observed whenever other animals are in the area and seems to indicate a concern of the male.
 

Ejaculation

Ejaculation in camelidae appears to occur throughout nearly the entire duration of copulation, which can vary from 1 to 65 minutes. In addition, semen could be collected from alpacas in as early as 5 minutes.^{(37, 54, 58, 59)} In the dromedary, we have found that conception is possible even when duration of copulation is less than one minute. However, high ovulation and copulation rates are attained only if the copulation time is at least 4 minutes (Table 3 ).

The dromedary displays multiple distinct periods of pelvic thrusting, gluteal muscle contractions, and semen discharge during copulation.^{(50, 67)}

Contractions of the ischiocavernous, bulbospongious and urethralis muscles surrounding the pelvic urethra may be correlated with ejaculation in the llama.

Measurements of urethral pulses taken during copulation of llamas show that they increase after 4 minutes into copulation and occur in clusters every 1 minute. Each cluster lasts 20 seconds and is composed of 4 to 5 rapid urethral pulses followed by a tremor of the whole body. Each cluster is preceded by 2 repositions and 38 pelvic thrusts. The authors have interpreted the urethral pulses accompanying the whole body strain as a single ejaculation. Thus ejaculation in the llama starts at about 4 minutes after the beginning of copulation and occurs every minute (18 to 19 ejaculations per 22 minutes).⁽⁵⁸⁾ This model of ejaculation is consistent with observations of ejaculation in other camelids.^{(49, 50, 54)} These observations (multiple ejaculation and straining during ejaculation) are confirmed by the pattern of ejaculation observed during semen collection by artificial vagina.^{(58, 59)}

We have made the same observations in the dromedary, using both a regular artificial vagina and also using just hand pressure. Straining of the body in the camel accompanied by an extension of the neck usually signifies occurrence of ejaculation. Fibroscopic evaluation of the cervix before and after breeding allows us to show that semen is deposited partly intra-uterine and partly intra-cervical or vaginal (Figure 2.14).

It is suggested that semen deposition in the alpaca is intracornual, close to the utero-tubal junction and that the penis moves back and forth from one horn to the other during copulation. The corkscrew shape and cartilaginous constitution of the glans penis allow dilation of the cervix and intrauterine deposition of semen.⁽¹⁹⁾ During copulation, llamas and alpacas produce a low guttural sound as air is expired through the mouth while the cheeks are inflated. Males can display all copulatory behavior without achieving intromission.^{(34, 36, 37)}

According to Chen et al.,⁽²⁷⁾ ejaculation takes place several times during copulation (dribbling) and semen is deposited in the anterior end of the vagina in the Bactrian camel.

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