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REPRODUCTIVE PROCESSES IN CAMELS (Camelus dromedarius) Yagil R. Faculty of Heal Sciences, Ben-Gurion University of the Negev, Beersheva

Introduction
A review on camel reproduction is not only a question of presenting new data associated with a specific subject, but is a move away from anecdotal data taken from nomadic camel herders (1) with their uncertain husbandry methods, via the model camel farm (2) where the scientists were also the farmers, to high-tech scientific laboratories (3).
As with all mammals, camel reproduction is adapted to its specific behavioral, anatomical, physiological and endocrinological peculiarities. The camelids inhabit the most extreme climates on the globe and their process of multiplication is determined by the availability of food and protection for the newborn, consequently their reproduction is governed by these factors. Camelids are found high in the Andes mountains of South America (New World camelids), in the frozen Gobi desert in Asia (Bactrian camels), and in the hot deserts of Africa and Middle East (Dromedaries). This review will deal with the reproductive performance of the dromedary, the one-humped, hot-desert camel.
As mammals are characterized by milk secretion lactation is an integral part of the reproductive cycle, and this will be discussed in another article.
Anatomy:
Note: all measurements will be affected by age, season, size and weight.
Male
Testes (4,5): They are found lying horizontally in the perineal region. In young males they are barely visible in the non-breeding season. In older males they are small and located almost completely between the legs. A faint median raphe divides the two testes. Between the ages of 6-10 years, its length averages 9cm, breadth 5cm, thickness 4.3cm and weight is 92grams. The right testicle is slightly smaller. In the rut season the testes become enlarged and protrude.
Penis (5): A cylindrical organ directed posteriorally. It is possible that this position prevents contact between the organ and the hot desert sand when the male squats, keeping the penal area above the sand. There are three groups of penal muscles: anterior, posterior and lateral. The contractions and relaxation of these muscles pull the penis forward during the breeding processes. The glans penis is curved along its ventral plane, giving it a hooked appearance.
It is noteworthy that the diameter of the penis decreases from its root towards the thin tapered glans penis. During erection the differences in diameter give the impression of opening of an old-fashioned telescope.
Female
In general the female genital tract is more similar to that of a mare than of a cow. The sizes are determined by the age of the animal. Externally the two uterine horns are joined but there is a definite median septum (6). The left horn is well developed while the right one is rudimentary. There is a short cervical canal and the mucosal folds are arranged in 3-4 rows. The cervix tends to protrude into the vagina, creating a dorsal and ventrical blind sac. The vagina is about 31 cm long. The vulva is about 8cm long, and a suburethral diverticulum with the urethral orifice above is in its ventral floor.
The sizes of the ovaries are determined by the age, size, health and stage of female cycle. Follicles on the left ovary are generally larger than those of the right one.
When palpated rectally the ovaries can be found close to the cervix.
Behaviour:
Male
The Dulaa is a palatal flap that is extruded on the side of the mouth during the mating season (5). It is incorrectly assumed that this protrusion is the tongue. The flap is formed under the influence of testosterone, so the more virile the male, the longer is its dulaa which protrudes further in a ball-like structure. The male normally takes a deep breath and when the air is expelled it pushes the dulaa out of the mouth, the nostrils quiver and there is a typical sound of “bloo, bloo, bloo” and a large secretion of saliva. After a few seconds the dulaa collapses and the sac is withdrawn into the mouth. The importance of the dulaa is that its formation is correlated to the amounts of testosterone in the blood; the size is an indication for the females of the male's virility. Towards the end of the season the typical sound is made but no dulaa appears.
The poll glands are situated on the back of neck between ears. They secrete a copious, acrid-smelling secretion, which flows down the back of neck, marking the skin with a dark color. The males rub their necks on any solid object, thus marking their territory. Laboratory examination of the poll gland secretions revealed similar concentrations of androgens as in the blood (5). Histological examination confirms that the poll glands are of endocrinological origin (7).
Urination: Another peculiarity of the male in rut is spreading its legs, placing its tail between them, urinating on it and then swishes it over its back. (4, 8, 9), It is likely that pheromones in the urine attract the females.
Aggressiveness: When the males exhibit all the above signs they become very aggressive towards other males and can attack humans, even their owners (6, 9).
It is noteworthy that male elephants in the musth exhibit similar behavioral signs to those of the camel (10).
Female: In the breeding season the female is receptive to the male for 3-4 days at a time, followed by about 10 days of quiet. This corresponds with the fluctuations in sex hormones in blood (11). When in rut the female approaches the male, presents her hind parts and urinates constantly and flaps her tail up and down in quick, short movements (4, 9).
Physiology:
The rut is confined to the cooler and wetter seasons, corresponding to the availability of food when the calf is born (11). In Israel this period is between end of December and end of April. At the equator the reproductive cycle can be all year round but particularly in the heavy rain season (4). When camels are kept corralled and have ample amounts of food, this period is extended by as much as 2 months (7, 12).
Male: In nomadic herds the male become sexually mature at about 5 years old (1), but this age declines when herds are better controlled (7)
Female: Females become mature at 4 years and remain fertile for over 20 years. This age is reduced as the husbandry practices improve and if the animals are kept in feed lots (12).
Inter-calf period: This is definitely dependent on husbandry practices. In nomadic herds the period is normally once very two years, but this is because the lactating females are separated from the herd in order to be close to humans. Therefore they, only mate in the following season (one year hence). As she-camels can have estrus 25-40 days after parturition they can give birth once a year (7, 12). The herders' misconception of selection led to “negative selection” for milk production in bringing poor milkers to the male soon after parturition, whereas good milkers gave birth once every two years (12).
Sexual cycle: Follicles take about 6 days to develop. The Graafian follicle can remain from 5 to 19 days and then regress over another 7 days. There is an estradiol peak every 7 days. The cycle is dependent on mating so there is an induced ovulation. Ovulation occurs 36 hours after mating (13,14). The corpeus luteum (CL) is flabby at the beginning of a pregnancy but becomes hard eventually. There can be as many as three CL in an ovary.
Endocrinology:
In females, an estradiol cycle is found only if there is no ovulation (13, 14). After copulation there can be a short-lived rise in progesterone. When the females are pregnant the progesterone levels rise to above 2ng/ml (9,15) In males there are elevated testosterone levels in the rut period.
Courting and mating:
In the rut period, males continually sniff about the females. When a female is “in heat” the male shows Flehmen and becomes excited (4, 5) . The male starts to push on the female to bring her down, which normally results in the female running away. The male gives chase, biting at her sides, back, legs, hump, or even genitalia. This often leads to severe wounds requiring surgery. When she eventually stands still, the male places his neck on hers and forces her to squat.
Then the male straddles the female, moves up to the hump and then begins to slide down until he eventually squats on the female, his front legs closely holding her, his full force on his tibiae (back legs).
Now the penis is pulled forward, the tip appears and it “feels around” for the vulva. When it is located the full length is inserted, one part after another. The male makes constant shuffling movements to push in further. He sits gazing into the distance, saliva trickling out of his mouth and a constant vibration of his nostrils. The female normally does not lie quiet but bellows and constantly bites his neck.
Mating can last up to 40 minutes and pulsations can be seen on the penis. When the male is finished he often just falls over on his side before standing up.Males can mate eight females in a day.
Semen: The semen is jelly-like and opaque (16, 17). The sperm are almost motionless. In the female genital tract the sperm become motile, an important fact since ovulation occurs only 36 hours after mating. If this is not known, examination of semen can mislead the observer in assuming the sperm are dead and the male is infertile.
Pregnancy:
It is assumed that the fertility rate in camels is low but this is normally due to the practice of bringing the male only once to the female. As it is not certain at what stage of the estradiol cycle the female is in, it is better for the male to mate the female once a day for a few days (16,17).
When a female is pregnant, she will show it by lifting and curving her tail when a male advances. The male then moves off looking for another, receptive, female. This is the method used by nomads to determine pregnancy in she-camels. Modern methods for pregnancy diagnosis include ultrasound (17), a bioassay with mice (18), or radioimmunoassay for progesterone (13).
As mentioned, calving once every two years is a managerial problem and not an endocrinological one (9, 19).
Gestation:
The length of pregnancy averages 1 year (308-440 days) but will be affected by the herders who determine the date that it conceives.
Parturition:
The signs of parturition begin a few hours prior to the appearance of the calf (12). The mother becomes agitated, gazes into the distance and moves away from other camels. Corralled camels can even attempt to break out.The first outer signs are the relaxation of the sacrosciatic ligaments, creating grooves on either side of the tail. The vulva becomes markedly swollen. When the cervix is fully dilated, in about 3-5 hours, the birth process begins. The female can remain standing, lie on her side or alternate between standing and lying.
The long front legs are the first to appear, followed by the head and shoulders. The rear portion is then rapidly ejected. The entire process normally lasts about 25 minutes. The placenta can be discarded immediately but normally only after an hour.
In some camels at the beginning of the birth process, the mother raises a leg and suckles herself, a “natural” way to raise oxytocin secretion, and hence uterine contractions.
As soon as the calf is out the mother stands,and in so doing,sever the umbilical cord.
female camels do not clean the calf or eat the placenta but are very protective mothers.
There are no reports of twins although aborted pregnancies can expel two foeti.
The placenta is similar to that of a horse, it is diffuse and smooth, with no cotyledons. There is an extra fetal membrane which is epidermal in origin which completely encloses the fetus (18).
The weight of the calf varies between 25 kg to 52 kg. Males are slightly heavier.
The calves normally stand after 30 minutes, but one hour is also normal. After another hour the calf starts looking for the teats, often helped by the mother.
When the commercial value of camels became apparent, modern reproductive interventions were introduced. The commercialization varied from racing camels in the Emirates (14, 17) to improving lactation performance in Israel (16).
Artificial insemination: is practiced in camelids. The peculiarities of the male and female reproductive processes must be taken into account. A modified bull vagina is used to collect semen. About 320 x 106 spermatoids are inseminated into the uterus 24hrs after GnRH treatment. The recipient must be induced to ovulate for a pregnancy (20).
The techniques of embryo transfers were developed for raising better racing camels in the Emirates (17) but also for increasing milk potential for starving Africa (16). In the Emirates the technique was developed in modern facilities with excellent equipment. In Israel the technique was developed in simple facilities, suitable for African conditions. In the well-equipped laboratories scanners were used to determine ovarian activity while in the other case reliance was placed on knowledge of the female cycle and using progesterone ear implants to bring the cycles to a starting point, before initiating hormonal treatment to get poly-ovaries. The females are mated at least twice on consecutive days or 48 hrs apart. Embryos were collected by transcervical uterine flushing 7 days after ovulation. Embryos were drawn into straws for later transfers. Recipients were treated with GnRH and 6 days after ovulation the embryos were transferred intrauterinely into the left, better developed, uterine horn.

Lactation:
This is an important part of reproduction because without milk there will be no “future generation”. The female starts producing small amounts of colostrum soon after parturition. The colostrum is pure white but very sticky (6).
It is common practice that if a calf dies, camel herders will either remove the skin and put it on a child, or tie the hind part of the calf around the mother’s flank as the she-camel will turn to smell her calf before “dropping” milk. No other calf will be allowed to suckle.

Acknowledgements:
The author is grateful to the Benny Slome Charitable Foundation for financial and morale support.

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