Reproductive Physiology in Male Camels
A good knowledge of the physiology of reproduction is the key element to good management of a species and to understanding infertility and the rationalizing of its treatment.
Puberty in the male is generally defined as the time when he is capable of successfully mating a female and getting her pregnant. In the dromedary there are no studies that define the exact age of puberty but field observations suggest that it is reached between 3 - 5 years old [1,2] and sexual activity can continue until 20 years of age , but this can vary due to different breeds of camels, genetics, nutrition and climatic changes. In the Bactrian puberty is generally reached by 4 years and sexual activity declines after 15 years of age, although some may continue until they are 20 years old [4,5].
Seasonality in the male is evidenced by changes in sexual behaviour, morphology and function of the genital organs, as well as changes in endocrinological profiles. Given the wide geographical distribution of the camels the breeding season is very variable but generally coincides with the period of low humidity, low temperature, and increased rainfall [6,7].
In India the breeding season (sometimes described as the rutting season) continues from late September to March, in Saharan and sub-Saharan regions it runs from October to May [8,9] and in the Middle East if goes from late October to late April. However, the onset of the rutting season can also be affected by the type of management and the individual male. Males that are loose in a herd tend to come into rut earlier and remain in season for a longer period than confined males .
It has been suggested that seasonal behaviour is more pronounced in the Bactrian camel lasting throughout the winter and into early spring with the dominant males starting their activity earlier than young and subordinate males .
Anatomical Evidence for Seasonality
Anatomical evidence is well illustrated by the increase in size and activity of the testis and accessory glands during the coolest months of the year. Histological studies of the testes also show increased spermatogenic and secretory activity during the rutting season. [11,12]. However, the most obvious change in the dromedary during the rutting season is the increased secretory activity of the poll glands giving the characteristic smell of the rutting male. Poll gland weight can increase from 40 - 100 g in the non-breeding season to 200 - 240 g in the rutting season. .
Endocrinological Evidence for Seasonality
Endocrinological evidence is shown by the increased secretion of androgen, especially testosterone. In Morocco, for example, testosterone levels increase from 2 ng/ml in October to 24 ng/ml in January and return to 4 ng/ml in May . This higher testosterone levels in the rutting season may be due to increased synthesis and release of testosterone either by an increased sensitivity of Leydig cells to LH, or an enhanced secretion of LH from the pituitary gland or both [14,15].
Pituitary and circulating Follicle Stimulating Hormone (FSH) levels are significantly affected by season. The highest concentrations are reached during winter and tends to drop reaching a minimum in summer before increasing again in Autumn. Although no significant changes were observed in circulating or hypopysal LH the highest frequency and amplitude of LH pulses were seen in males during the cooler months (December - January) .
Serum prolactin levels are high during the non-breeding season and decrease significantly in the rutting season. [16,17], thus it was proposed that hyperprolactinemia may cause reduced fertility and libido in the male dromedary during the non-breeding season probably due to its inhibitory action on the synthesis and secretion of FSH and LH .
The male dromedary becomes increasing aggressive towards other males, and sometimes even towards people, during the breeding season. Males that are confined show increased pacing and anxiety and may make several attempts to break out of the corral or pen. If they are kept with females they spend most of their time guarding the herd and surveying it for the presence of other strange males. Because of this continuous stress there is a reduction in food intake and frequent diarrhoea resulting in a loss in weight - sometimes up to 35%. Aggressive behaviour has also been described in Bactrians, as often males in a free ranging herd chase each other and engage in fighting that leads to serious injuries .
Soft Palate Ejection
Sexual behaviour is also characterized by exteriorisation of the soft palate, known as the dulah (Fig. 1), but this has only been described in dromedaries not Bactrian camels. The protrusion of the soft palate occurs all day long at intervals of 15 - 30 minutes and is accompanied by loud gurgling and roaring sounds. The protrusions become more frequent with increased excitement such as the presence of other males and females [2,10].
Figure 1. Male camel extruding his soft palate (dulah) when sexually aroused. To view click on figure
During copulation the soft palate ejection may be replaced by grinding of the teeth and frothing at the mouth. This frothing is generally attributed to increased secretion of the salivary glands and the frequent exteriorisation of the soft palate [10, 18].
This is one of the main sexual behaviours exhibited during the breeding season. It generally takes on two forms: that of (i) urine spraying and (ii) smudging of poll gland secretions.
This behaviour is generally increased in the presence of another male or when females are passing nearby. During urine spraying the dromedary assumes the crouched urination posture and urine is ejected towards the back in small quantities and spread over the croup of the animal and surrounding areas with regular tail beating as shown in Fig. 2. The tail is held under the prepucial 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 spraying activity is continued throughout the day and often the skin over the sacral region becomes dark and thickened due to the formation of a crust of mixed urine and sand .
Figure 2. Male rutting behaviour. Note the crouched urinating position of the male with widely spread hind-legs and the tail beating up and down to spread urine over the croup. To view click on figure
Smudging is used to disseminate the secretions of the poll gland. The secretions are light brown/amber in colour when first excreted but become tarry and dark after a few minutes. It can easily be seen dribbling down the neck of the male and has a very strong foetid smell (Fig. 3). The area corresponding to the poll glands becomes large and darkened due to this increased activity. These secretions probably contain androgens and 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 to disseminate the secretions. The Bactrian camel also exhibits these marking behaviours.
Figure 3. The active poll gland (arrow) of the male dromedary. Note the tary dark secretions trickling down the side of the neck. To view click on figure
During the breeding season males continue to seek receptive females. They sniff the perineum and flank of the females and frequently display a flehmen reaction [7,9]. Males that roam freely with females will often chase them and force them to sit down by putting pressure on the neck and biting the hump, even if they are not receptive. This obviously contributes to their weight loss during the season.
Mating is carried out with the female sitting in sternal recumbency and the male squatting behind her with his hind legs flexed and his forelegs extended on either side of the female as seen in Fig. 4. The duration of copulation can vary and tends to decrease as the weather becomes warmer. On average dromedaries mate for 5.5 minutes but this can range from anything between 3 - 25 minutes . Bactrians tend to mate for less time i.e. on average 3 minutes but can be as long as 10 minutes [4,5].
Figure 4. Copulation in camels takes place in the crouched position. The male continually grinds his teeth and dribbles copious amounts of saliva over the female. To view click on figure
Erection is only achieved after the female is mounted in a sitting position and the penis is not fully extended until after intromission is complete. Ejaculation appears to occur almost throughout the entire duration of copulation. 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 has shown that semen is deposited partly intra-uterine and partly intra-cervical or vaginal .
Reproductive Physiology in Female Camels
The reproductive efficiency of the female camel is low in comparison with other domesticated animals. This is probably due to the delay in the onset of puberty, the increased age at first conception and the long interval between births .
Sexual activity in dromedaries and Bactrians has been reported to start as early as 2 - 3 years of age but usually they are not bred until they are 4 years old. There are several factors that can influence the age of the onset of puberty, such as nutrition, season of birth and breed of camel. The most important factors being the nutrition and adequate growth, as these seem to influence the onset of ovarian activity and chances of conceiving and carrying the pregnancy to term. If females are bred before they reach 70% of their adult body weight they run a greater risk of abortion .
Induction of puberty at as early as 1.5 - 2.5 years has been attempted by several people using single or multiple injections of equine Chorionic Gonadotrophin (eCG: 1000 - 7000 i.u.; Folligon) but even though the majority of females responded to such treatment, the incidence of early embryonic death was high [24,25]. In addition, the calves born to eCG treated females lagged behind in their growth and development up to 14 months of age. Thus trying to advance the age of first conception using this treatment cannot be recommended.
Both the dromedary and Bactrian are regarded as seasonal breeders, with a relatively short breeding season, based on the seasonal distribution of births and on the status of ovarian activity in slaughtered animals [26-28]. Outside of the breeding season mating activity ceases and the ovaries are inactive or only have a few, small follicles. However, there seem to be rather conflicting reports as to the beginning and length of the seasonal activity in the dromedary, but as a rule, increased breeding activity has been reported to occur in March and August in Sudan,  December to March in Pakistan , December to April in Egypt [27,28] and from November to April in most of Arabia [31,32]. This is generally during the period of low climatic temperature, rain and better grazing conditions. The breeding season for the Bactrian camel in China has been reported to occur between mid January and mid April. In the United Arab Emirates, well fed and watered animals show ovarian activity all year round and the determinate factor of the seasonality in conception dates are due to a decrease in libido of the male and an increase in early embryonic death during the summer months .
Endocrinological Aspects of Seasonality
There is limited information on the endocrinological aspects of seasonality focusing mainly on oestrogen and Luteinizing hormone (LH) levels. Plasma levels of oestradiol - 17β very considerably from one month to another but there does not seem to be any association between the level of this hormone and their breeding activity [33,34]. Concentrations of LH are higher during the breeding season than during the non-breeding season [33,34] as during the breeding season the pituitary is more sensitive to and releases more LH after Gonadotrophin Releasing Hormone (GnRH) challenge [35,36].
Several people have described the signs of oestrous behaviour in the dromedary as being: mounting other females, restlessness, swelling of the vulva, straddling the hind legs and urinating, vaginal mucus discharge and receptivity to the male as shown in Fig. 5. When displayed, oestrous behaviour lasts on average 4 - 6 days, but can vary from 1 - 21 days [26,29]. However, all these signs are very variable in duration and intensity, and are therefore unreliable for the detection of oestrus.
Figure 5. Oestrous behaviour in the female dromedary. Note the raised tail and the flehmen reaction of the male after sniffing her urine and vulva. To view click on figure
The proportion of females displaying strong oestrus behaviour is usually small and not all the females will show all these signs, despite the presence of a mature follicle. Also, receptivity to the male can be displayed by females with no follicles in the ovaries and for up to 7 days after ovulation or when pregnant and progesterone levels are high [29,32]. Oestrous behaviour therefore cannot be used reliably to decide the timing of breeding in the dromedary .
In the Bactrian camel the length of the oestrous cycle is variable but tends to be longer in multiparous than in primiparous females. The period of receptivity (2 - 8 days) and the signs of oestrus are similar to those reported for dromedaries and tend to be shorter in lactating females [37,38].