www.elsevier.comrlocateranireprosci
Reproduction in Old World camels
M.M. Al Eknah
)Camel Research Centre, College of Veterinary Medicine and Animal Resources, King Faisal UniÕersity,
P.O. Box 1757, Al-Ahsa 31982, Saudi Arabia
Abstract
The article reviews aspects of the basic reproductive biology of the camel, such as puberty, breeding season, ovarian dynamics, synchronisation of ovarian activity and artificial insemination, and superovulation and embryo transfer. Pregnancy and parturition are also discussed.q2000 Published by Elsevier Science B.V. All rights reserved.
Keywords: Camel; Reproduction
1. Introduction
Ž .
The genus Camelus has two species — the dromedary or Arabian camel one-humped
Ž .
and the Bactrian camel two-humped . They are artiodactyl mammals in the pad-footed suborder Tylopoda. It appears probable that dromedaries and Bactrian camels were domesticated separately. The domestication of the dromedary occurred in the Arabian peninsula, while Bactrian camels were first domesticated in Mongolia. From the physiological point of view, dromedaries exhibit certain characteristics that enable them
Ž .
to survive in arid regions Epstein, 1971 .
Full exploitation of the camel’s production of milk and meat will only be possible
Ž .
when the reproductive performance is improved Yagil, 1985 .
2. Puberty
Camels mature late. The female camel usually reaches puberty at 3–4 years of age ŽLeese, 1927; Evans and Powys, 1979; Shwartz, 1992; Musa et al., 1993 . However,.
Ž .
females are not bred until they are 5–6 years old Matharu, 1966 . Male camels reach puberty at about 3 years, but full reproductive activity is not developed until they are
)Corresponding author.
0378-4320r00r$ - see front matterq2000 Published by Elsevier Science B.V. All rights reserved.
Ž .
Ž .
6–7 years old Novoa, 1970; Arthur et al., 1985 . Inadequate body weight caused by Ž lack of sufficient food appears to be the cause of delayed puberty in the camel Chatty,
.
1972 . Nutrition seems to play a vital role in the various physiological events for the attainment of sexual maturity and in the reproductive process. The faster an animal
Ž .
grows, the earlier it will reach sexual maturity Maynard et al., 1979 . In cattle, puberty
Ž .
occurs at a particular liveweight bodyweight or body size rather than a fixed age. Meanwhile, in sheep, it is complicated by their seasonal breeding pattern in Europe ŽMcDonald et al., 1988 . Undernutriton delays puberty in both male and female virgin. camels and, if severe, can cause retrogressive changes in the sexual organs after their
Ž .
full development Maynard et al., 1979 .
3. Breeding season
Camels are considered seasonal breeders. However, information about the breeding season in the dromedary is rather conflicting. Thus, the breeding season has been
Ž .
reported from March to August in Sudan Musa and Abusineina, 1978a , December to
Ž . Ž
March in Pakistan Yasin and Wahid, 1957 , November to March in India Matharu,
. Ž . Ž
1966 , April to May in Somalia Mares, 1954 , December to May in Egypt Shalash,
. Ž .
1965 , December to March in Tunisia Minoia et al., 1992 , and October to April in
Ž .
Saudi Arabia Abdel-Rahim and El-Nazier, 1990; Al-Eknah et al., 1997a,b . Decreasing Ž
daylength appears to be the stimulus to seasonality Merkt et al., 1990; Musa et al.,
. Ž
1993 . In camels near the equator, factors such as rainfall Bono et al., 1989; Arthur,
. Ž .
1992 , nutrition, and management Wilson, 1984 may override the effects of
photope-Ž .
riod and allow breeding to occur throughout the year Arthur et al., 1985 . Therefore, Ž
with a continuous supply of sufficient food, camels can be truly polyoestrus Arthur et .
al., 1982 . The main trigger for Arabian camel sexual receptivity is rainfall and the
Ž .
subsequent availability of improved nutrition Cristofori et al., 1986 . Mature male dromedary camels show also a seasonal sexual activity. The rutting season occurs during
Ž .
spring in Egypt Abdel-Raouf and El-Naggar, 1964 , from November to February in
Ž .
India Khan, 1971 and from mid-January to the end of May in the Turkiman dromedary ŽAbdunazarov, 1970 . Higher testosterone levels and active poll glands have been found.
Ž
during the rutting season Yagil and Etzion, 1980; Tingari et al., 1984; Agarwal and .
Khanna, 1990 . Spermatogenesis continues throughout the year in male camels, but at a
Ž .
higher rate during the cooler months of the breeding season Abdel-Raouf et al., 1975 . Hyperprolactinaemia has been proposed to cause reduced libido and fertility during the nonbreeding seasons of the male camel, due to the suppressive effect of the high
Ž .
prolactin levels on secretion of FSH and LH Azouz et al., 1992 . GnRH treatment has been used to stimulate sexual activity in normal males outside the breeding season ŽMoslah et al., 1992 ..
4. Ovarian dynamics
Camels are seasonally polyoestrus and induced ovulators. Follicular growth occurs in
Ž .
Ž
that of ungulates and primates, is incomplete, consisting of prooestrus growing
folli-. Ž . Ž
cles , oestrus mature follicles , and dioestrus follicular atresia if mating has not .
occurred . During the breeding season, waves of follicular growth, maturation, and
Ž .
atresia occur constantly in both ovaries Musa, 1969; El-Wishy and Hemeida, 1984 . Ž .
Al-Eknah et al. 1993 recorded four distinct phases of uterine activity during the oestrous cycle of the Saudi camel: the high phase, declining phase, low phase and increasing phase. These phases correspond to follicular, atretic follicular, nonfollicular
Ž .
and growing follicular stages, respectively Nawito et al., 1967 . The mean duration of
Ž .
the oestrous cycle has been reported to be 23.4 days in India Joshi et al., 1978 , 24.2
Ž . Ž
days in Egypt Nawito et al., 1967 , and 28 days in Sudan Musa and Abusineina, .
1978b . The latter investigators recorded an oestrous duration of 4–6 days and 6 days Ž2–14 days of follicular maturation. The follicles maintain their size for 13 days 5–19. Ž
. Ž .
days and then regress in 8 days 7–10 days . In Saudi Arabia, oestrous-cycle durations Ž . of 16–30 days and 11–27 days have been observed by Bakkar and Basmaeil 1988 and
Ž .
Al-Eknah et al. 1993 , respectively.
Realtime ultrasonography has been used to monitor the ovarian follicular wave
Ž .
pattern in the camel Skidmore et al., 1996 ; the follicular cycle has been divided into a
Ž . Ž .
growth phase 10.5q0.5 days , a mature phase 7.6q0.8 days and a regression phase Ž11.9q0.8 days . Serum oestradiol concentration reaches peak values when the domi-. nant follicle measures 1.7q0.1 cm in diameter. The optimal time to mate or attempt to induce ovulation is when the growing follicle measures 0.9–1.9 cm in diameter ŽSkidmore et al., 1996 . Ovulation in the camel is induced and occurs after mating. ŽNawito et al., 1967; Novoa, 1970; Musa and Abusineina, 1978b; El-Wishy and
.
Hemeida, 1984; Cristofori et al., 1986 . The evidence of induced ovulation is the
Ž .
absence of a corpus luteum formation Nawito et al., 1967; Elias et al., 1984 and low
Ž .
serum progesterone concentrations in unmated females Skidmore et al., 1996 . The latter investigators have reported that no spontaneous ovulation occurs in camels, even in females that are close to, but not mated by, male camels. Ovulation can occur within 48 h following mating or intramuscular injection of luteinizing hormone; the left and right ovaries function alternatively. In the absence of a male, oestrous may last 2 weeks, whereas if copulation occurs on the fist day of oestrous, receptivity may disappear after
Ž .
3 days Musa and Abusineina, 1978b .
5. Synchronisation of ovarian activity and artificial insemination
Application of artificial insemination in the camel requires a reliable method for synchronisation of oestrus in groups of females. Such a method is also essential in embryo transfer programmes. Extensive research and development have been achieved in oestrous synchronisation and controlled breeding in cattle; however, little research has been found in the camel side. Camels as induced ovulators offer great prospects of natural synchronisation of oestrous, since with copulation follicular regression occurs in
Ž .
3 days Yagil and Etzion, 1984; Yagil and van Creveld, 1990; Musa et al., 1993 . The synchronisation of oestrous has solved problems of oestrous detection and has made
Ž .
Ž .
progesterone-releasing intravaginal device PRID has been used to synchronise ovula-Ž
tion in a significant proportion of female camels Cooper et al., 1990, 1992; Skidmore et .
al., 1992 . The devices are withdrawn after 7 days, to mimic the camel’s luteal phase. Ž .
According to Cooper et al. 1992 , the PRID alone was not a satisfactory method for controlling ovarian function. Progestin injections have been successfully used to
syn-Ž .
chronise oestrous in the dromedary Mckinnon and Tinson, 1992 . Equine chorionic Ž .
gonadotrophin eCG , in doses ranging from 1000 to 8000 IU, has been used to induce oestrous in both the nonbreeding and breeding seasons. However, the number of
Ž
pregnancies achieved has been found to be very low Yagil and Etzion, 1984; Elias et .
al., 1985; Rai et al., 1990 .
Efficient methods to induce and synchronise ovulation in the camel are now required as the interest grows in the potential application of artificial insemination and embryo
Ž .
transfer Cooper et al., 1992 . In the camel, ovulation could be induced by mating with
Ž .
an intact or vasectomised male Marie and Anouassi, 1987 . However, manual stimula-tion of the cervix, as well as the intrauterine injecstimula-tion of whole semen, seminal plasma, water, or prostaglandin, have not been found to stimulate the release of sufficient LH
Ž
from the pituitary to cause ovulation Musa and Abusineina, 1978a; Sheldrick et al., .
1992 . Mechanical stimulation of the cervix, which triggers ovulation in species such as Ž
the cat and rabbit has not been useful to induce ovulation in the camel Musa and .
Abusineina, 1978b; Musa et al., 1990; Elias et al., 1984 . Therefore, the ovulatory response in the camel could be the result of a combination of stimuli, including a chemical factor in the seminal plasma, neurohormonal responses to the mechanical
Ž
stimuli of coitus and the male effect Marie and Anouassi, 1987; Anouassi et al., 1992; .
Moslah et al., 1992; Skidmore et al., 1996 .
Ovulation in the camel has been induced by a single treatment with GnRH or hCG ŽMarie and Anouassi, 1987; Anouassi et al., 1992; Mckinnon and Tinson, 1992;
.
Sheldrick et al., 1992; Skidmore et al., 1996 . The latter investigators have postulated that ovulation rates reached 85% in natural mating, 81% with 20 mg GnRH analogue, and 67% with 3000 IU hCG when the dominant follicle measured 0.9–1.9 cm in diameter. A marked reduction in the effectiveness of natural mating and these hormones to induce ovulation has been observed when the diameter of the dominant follicle
Ž .
exceeded 2.0 cm in diameter Skidmore et al., 1996 . Ž .
Artificial insemination AI is a tool for improving genetic traits, such as milk, meat, and wool production and racing ability. This is performed by using superior male genomes on population basis. Camel semen deposited into the female’s uterus may
Ž .
induce ovulation without the need for coitus Chen et al., 1985; Musa et al., 1990 . This makes AI an attractive tool for genetic improvement, using selected males and
insemi-Ž nating groups of females in which follicular development has been synchronised Musa
.
et al., 1993 . Semen can be collected from males either by using an artificial vagina ŽAV. during mating or by electro-ejaculation. A bull AV and a standard bovine
Ž
ejaculator have been used to collect semen from the male camels Abdel-Raouf and El-Naggar, 1976; Tingari et al., 1986; Dafalla et al., 1988; Sieme et al., 1990; Anouassi
.
et al., 1992; Musa et al., 1993 . Camel semen is thick and gelatinous immediately after Ž
collection. Liquefaction time varies from 4.5–9.6 min Abdel-Raouf and El-Naggar, .
325=106rml and percentages of motile sperm, dead sperm, and abnormal sperm Ž
higher than 50.5%, lower than 18.0%, and lower than 27.7%, respectively Tingari et al., .
1986; Ismail, 1988; Merkt et al., 1990; Musa et al., 1992, 1993 . Billah and Skidmore Ž1992 reported a considerable variation in the semen characteristics of the dromedary. camel. Semen quality has been found to be correlated with the general health and the
Ž .
nutritional status of the males Musa et al., 1993 .
For liquid preservation of camel semen, various extenders that showed good results
Ž . Ž .
include laiciphose Cassou, 1959 , Androlepe Waberski et al., 1989 , sodium citrate
Ž . Ž .
egg yolk extender Kupper, 1954 , and the Dimitropolouse extender Rasbech, 1984 . Extenders containing egg yolk and lactose appeared more suitable to preserving camel
Ž .
semen in the liquid state Sieme et al., 1990; Anouassi et al., 1992; Musa et al., 1992 . Diluted fresh semen has been preserved in plastic tubes and stored at 48C for a
Ž .
maximum of 36 h Musa et al., 1993 . Deep freezing of camel semen has been Ž .
performed. Sieme et al. 1990 compared different freezing methods with recommended Ž .
modifications of the technique developed by Westendorf et al. 1975 . A major difficulty
Ž .
with camel AI is ensuring that the inseminated females ovulate Chaudhary, 1995 . Ž .
According to Anouassi et al. 1992 ovulation rates and pregnancy were significantly higher in inseminated camels that had been mated by a vasectomised male. However, this is not a practical method because of the risk of the transmission of venereal and other diseases. Therefore, following AI, ovulation has been induced with either 3000 IU
Ž .
hCG or 20mg of the GnRH analogue, Buserelin Mckinnon and Tinson, 1992 .
6. Superovulation and embryo transfer
The number of offspring likely to be produced by a prestigious female camel in her relatively short breeding life is inadequate to provide a good distribution of the desired
Ž .
genetic material Musa et al., 1993 . Due to the restricted breeding season and the camel’s long gestation period, judicious use of embryo transfer could increase
reproduc-Ž .
tive efficiency in this species Skidmore et al., 1992 . Embryo transfer is an established technique in large domestic animal species. However, little research on the camel has been reported. Synchronisation of ovulation in donors and recipients, and induction of
Ž
superovulation in donors, are challenges in camel embryo transfer Mckinnon and .
Tinson, 1992 . eCG has been used successfully in camels at various doses between 1500 Ž
and 6000 IU to stimulate the ovaries for the production of multiple follicles Anouassi .
and Ali, 1990; Skidmore et al., 1992; Mckinnon and Tinson, 1992 . Another method for superovulation is the use of 1–3 mg ovine FSH in a split dose regime over 3–6 days ŽCooper et al., 1990, 1992; Skidmore et al., 1992; Mckinnon and Tinson, 1992 . The. latter investigators collected more embryos from donors stimulated with pituitary FSH than with eCG. The gonadotrophin treatments were performed just before or after the
Ž .
removal of the PRID Skidmore et al., 1992; Cooper et al., 1992 or on the last day of
Ž .
the progesterone therapy Mckinnon and Tinson, 1992 . Donor camels were mated once or twice 12 h apart, or artificially inseminated. Ovulation was enhanced with hCG or
Ž .
to the exogenous gonadotrophin therapy varied tremendously between individual donors ŽAnouassi and Ali, 1990; Skidmore et al., 1992 . Synchronisation of oestrous in the. recipients has been tried using PRIDs, inserted into a large number of females and
Ž
withdrawn in 7–10 days to provide a pool of synchronised recipients Cooper et al., .
1990, 1992 . The recipients were also treated with either hCG or a GnRH analogue ŽBuserelin in order to enhance synchronous ovulations. Embryos were flushed from.
Ž
donor camels on Day 6 or 7 after mating Anouassi and Ali, 1990; Cooper et al., 1990; .
1992 . Nonsurgical embryo recovery has been performed in the camel using either a
Ž . Ž .
two-way Cooper et al., 1990 or three-way catheter Skidmore et al., 1992 . The latter investigators recommended the transfer of embryos to recipients that are 1 or possibly 2 days negatively synchronous with the donors.
7. Pregnancy and parturition
Ž .
In one of our studies Al-Bisher, 1998 , it was found that gestation length in the Ž
camel is 373–393 days. This is consistent with the findings of other authors Musa and .
Abusineina, 1976; Hermans and Shareha, 1990; Abdel-Raouf, 1993 . However, longer
Ž .
and shorter gestation periods have been reported Yagil and Etzion, 1984 . This variation in gestation length could be due to the method of husbandry, number of
Ž .
matings over the entire period of oestrous Novoa, 1970 , number of pregnancies, sex of
Ž . Ž
the foetus Agarwal et al., 1987; Arthur et al., 1982 , level of feeding Yagil and Etzion,
. Ž .
1984 , or season of conception Elias et al., 1991 . The accuracy in diagnosing pregnancy may help in determining the exact gestation length.
Ž
Plasma progesterone concentrations in camels remains constantly low Homeida et .
al., 1988 . Following mating, at least one corpus luteum is formed, secreting a significant amount of progesterone. In our study, a value of more than 2 ngrml was recorded during pregnancy. Although both ovaries equally produced ova, pregnancy occurred only in the left uterine horn. Embryos resulting from fertilised ova in the right horn must have migrated to the left horn for unknown reasons. The embryotoxic effect associated with the right uterine horn, an alternative that involves prostaglandin-F2a
-Ž .
mediated luteolysis has been suggested Fernandez-Baca et al., 1979 . Oestrogens are
Ž .
continuously secreted during pregnancy in the camel Agarwal et al., 1987 . At mid-gestation, oestrogen concentrations rise, suggesting continued follicular
develop-Ž .
ment during pregnancy El-Wishy et al., 1981; Wilson, 1984 . High concentrations of oestrogens in the allantoic fluid on the day of parturition have also been demonstrated in
Ž the camel, suggesting that the placenta could be a probable source of oestrogens Elias et
. al., 1984 .
The cervical plug has unique properties for sealing off the external cervical os during
Ž .
pregnancy in the camel Guyton, 1991 . The presence of the cervical plug is an indication of pregnancy in this species. The physicochemical properties of the cervical
Ž .
degree of hydration under the influence of progesterone, which leads to mucus concen-Ž
tration or alteration and arrangements, affects the low elasticity of the mucus Prasad et .
al., 1981 .
Parturition is a continuous process in camels, which could be elicited by hormonal changes. It appears that expulsion of the foetus in the camel is preceded by the attainment of a minimum level of plasma progesterone and high levels of oestrogen ŽElias et al., 1984; Al-Bisher, 1998 . The premonitory signs of approaching parturition. includes segregation from the herd, restlessness, increasing humming, and relaxation of
Ž .
the sacroisciatic ligaments Musa, 1983; Al-Bisher, 1998 . However, the presence of colostrum in the udder remains the best sign of approaching parturition in the camel, as
Ž .
in the cow and mare Arthur et al., 1985; Elias and Cohen, 1986 . Dilatation of the Ž
cervix during the peri-parturient period of the camel has also been described Al-Eknah, .
1996 .
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