Factors affecting reproductive performance in dromedary camel herds in Saudi Arabia
Ahmed Ali, Derar Derar, Abdulhadi Alsharari, Assaf Alsharari, Rashid Khalil, Tariq I. Almundarij, Yaser Alboti & Fahd Al-Sobayil Tropical Animal Health and Production ISSN 0049-4747 Volume 50 Number 5 Trop Anim Health Prod (2018) 50:1155-1160 DOI 10.1007/s11250-018-1545-3
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Author's personal copy Tropical Animal Health and Production (2018) 50:1155–1160 https://doi.org/10.1007/s11250-018-1545-3
REGULAR ARTICLES
Factors affecting reproductive performance in dromedary camel herds in Saudi Arabia Ahmed Ali 1,2 & Derar Derar 1,2 & Abdulhadi Alsharari 1 & Assaf Alsharari 1 & Rashid Khalil 1 & Tariq I. Almundarij 1 & Yaser Alboti 1 & Fahd Al-Sobayil 1 Received: 26 December 2017 / Accepted: 6 February 2018 / Published online: 15 February 2018 # Springer Science+Business Media B.V., part of Springer Nature 2018
Abstract A survey of 7122 dromedary camels in 115 herds in Saudi Arabia was used to estimate the effects of herd size (HZ; < 25 vs. 25– 49 vs. 50–100 vs. > 100 camels), herder/camels ratio (H/C; 1:< 25 vs. 1:25–50 vs. 1:> 50), manager experience (ME; < 5 vs. 5–10 vs. > 10 years), male/females ratio (M/F), housing system (HS; free vs. closed vs. mixed), length of the breeding season (winter vs. winter and spring vs. fall, winter and spring), age at first mating (3 vs. > 3 years), and time of mating after parturition (≤ 3 vs. > 3 months) and their interactions on the overall pregnancy rate. Barren females of these herds (n = 886) were examined for the causes of infertility. Results showed that herds with H/C of 1:< 25 had higher overall pregnancy rate (95.29%) than herds with H/C of 1:25–50 (79.84%) and those with H/C of 1:> 50 (72.79%) (p = 0.003). Herds having ME of > 10 years revealed greater overall pregnancy rate (94.89%) than herds with ME of 5–10 years (80.54%) and those with ME of < 5 years (72.5%) (p = 0.001). There were significant interactions between H/C × HZ (p = 0.003), H/C × HS (p = 0.006), and ME × HS (p = 0.02). The overall pregnancy rate did not significantly differ between herds bred females by age of 3 years and those bred females by age > 3 years and in females bred within 3 months after parturition and in those bred after 3 months. The mean calving interval was shorter (p = 0.008) in camels mated within 3 months of parturition (15.25 ± 2.8 months) than in those mated after that time (24.33 ± 6.5 months). Clinical endometritis, ovarian hydrobursitis, and vaginal adhesions were the common clinical findings in barren females. Thus, efforts to reduce the age at first mating and the interval after calving, increase the number of herders/camels, and control reproductive disorders could improve the reproductive performance and quality of camel herds in Saudi Arabia. Keywords Dromedary camel . Reproductive performance . Pregnancy rate . Saudi Arabia
Introduction Camels are important to the Saudi community as a source of meat and milk and as an extension of history and heritage. According to the report of the Ministry of Agriculture (2015), there are approximately 223,441 dromedary camels in Saudi Arabia. Reproduction is commonly the key to improved livestock performance. The management of reproduction in dromedary camel, worldwide, is still very important,
* Ahmed Ali
[email protected] 1
Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, Buraydah, Qassim 51452, Saudi Arabia
2
Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut 71526, Egypt
despite neglected, issue. Consequently, the implementation of strategies for introducing correct monitoring of fertility index and assisted reproductive technologies in camel herds would be strategic (Elwishy 1987; Skidmore 2011; Nagy et al. 2013). It has been widely suggested that the reproductive efficiency of the camel under natural conditions is low. These low reproductive rates are probably due to the delay in the onset of puberty, long gestation period, prolonged period of lactation, relatively short breeding season, endemic presence of some reproductive diseases, and high rate of early embryonic mortality (Nawito 1967; Djellouli and Saint-Martin 1992; Skidmore 2011; Ali et al. 2015; Khalafalla et al. 2017). The prospect of increasing the reproductive performance of camels may be impeded by the persistent use of traditional systems of reproductive management in most breeding herds (Al Eknah 2000; Almutairi et al. 2010; Skidmore et al. 2010). Enhanced feeding and management practices, disease control, and superior selection might, however, increase the productive
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and reproductive performance as well as the quality of camel herds (Yagil 1982; Skidmore 2011; Fatnassi et al. 2014; Ali et al. 2015). In traditional management systems, camels usually calve once every 2 years (Iwema 1960; Matharu 1966; Merkt et al. 1990), but with improved feed, they may calve every 18 months (Knoess 1977). Under the semi-intensive system in North Kordofan, Sudan, about 78% of females became pregnant in the fifth to eighth-month postpartum with the calving interval varying from 17 to 20 months. Under the traditional system, only 44.5% of females became pregnant in the 11th to 16th-month postpartum, and the calving interval varied from 23 to 28 months (Bakheit et al. 2016). Little information is available on the reproductive performance and the factors influencing it in dromedary camels in Saudi Arabia. The objective of this study was, therefore, to estimate the reproductive performance and effects of herd size; herder/animals ratio; manager experience, male/females ratio, housing system, and length of the breeding season, age at first mating, and time of mating after parturition on the overall pregnancy rate in dromedary camels raised mainly under natural condition in Saudi Arabia.
Material and methods
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pregnant females/total number of mated females) were also collected. Barren females of these herds (n = 886) were examined at the Veterinary Teaching Hospital of Qassim University for the causes of infertility. The reproductive tract of each animal was examined through standard transrectal palpation and by ultrasonography attached to a 5-MHz probe (Aloka Co., Ltd., Tokyo, Japan). Vaginal examination with a gloved hand was performed to estimate the patency of the vagina and cervix and to evaluate the nature of the vaginal discharges. Abnormal vaginal discharges (catarrhal, mucopurulent, purulent) were regarded as marks of clinical endometritis (LeBlanc et al. 2002; Sheldon and Dobson 2004). The animals in most of these herds were fed on crushed barley and dry berseem (Trifolium alexandrinum L.).
Statistical analysis The data were analyzed using the General Linear Models procedures of the SPSS program, version 24.0 (2016). The overall pregnancy rate was the dependent variable. The main effects in the model were herd size, herder/camels ratio, manager experience, male/females ratio, housing system, length of the breeding season, age at first mating, and time of mating after parturition. Means of calving interval were compared by t test. Differences in the percentages were evaluated by the chi-squared test. Significance was set at p < 0.05.
Animals and management Managers of 115 camel herds amounting to a total of 7122 camels were asked to complete a questionnaire about the reproductive efficiency of the camels in their herds. These herds were situated at different localities around the Kingdom of Saudi Arabia. The camel herds were gathered/sorted by the herd size (HS; < 25, n = 25 vs. 25–49, n = 38 vs. 50–100, n = 40 vs. > 100 camels, n = 12 herds), herder/camels ratio (H/C; 1:< 25, n = 24 vs. 1:25–50, n = 68 vs. 1:> 50, n = 23 herds), length of experience of the manager in camel herd management (ME; < 5, n = 15 vs. 5–10 n = 59 vs. > 10 years, n = 41 herds), male/females ration (M/F; 1:< 25, n = 28 vs. 1:25–50, n = 75 vs. 1:> 50, n = 12 herds), housing system (HS; free system [the camels were left unconfined in open desert areas, n = 40 herds] vs. closed system [the camels were kept throughout the day and night in pens of about ∼15–20 m2/head, n = 19 herds] vs. mixed system [the camels were left free during the day and kept in pens at night, n = 56 herds]), age at first mating (the age of female and male camels when mated for the first time in their life; 3 vs. > 3 years), and time of mating after parturition (≤ 3 vs. > 3 months). Data concerning pregnancy duration, weaning age, and the overall pregnancy rate (number of end-of-season
Results Many camel herds bred females at the ages of four (77/115 herds, 67%) years and fewer at the ages five (30/115 herds, 26%) and three (8/115 herds, 7%) years (Table 1). The overall pregnancy rate did not significantly differ between herds bred females by age of 3 years and those bred them later. The mean reproductive life of the females was 20 ± 4.5 years, during which they give birth to a mean number of 9 ± 2.7 calves. Most herds used the males for mating by the ages of five (69/115 herds, 60%) years and a few by the age of four (30/ 115 herds, 26.1%) and six (16/115 herds, 13.9%) years. Each male was allowed to mate with 3.14 ± 1.5 females per day, with an average of 36.29 ± 14.1 females per rutting season. Very few herds (n = 12) replaced the bull every 5 years, while the remaining herds kept the same bull(s) for life. Male/females ratio did not affect the overall pregnancy rate. The breeding season was reported as winter (n = 23/115 herds, 20%), winter, and spring (n = 71/115 herds, 61.7%) and fall, winter, and spring (n = 21/115 herds, 18.3%). The length of the breeding season had no influences on the overall pregnancy rate. Pregnancy duration did not differ between parities. In only few herds (n = 30/115, 26.1%) were the females mated within
Author's personal copy Trop Anim Health Prod (2018) 50:1155–1160 Table 1 Reproductive performance of dromedary camels in 115 herds containing 7122 animals
Reproductive parameter
1157
Mean
Std. error
Minimum
Maximum
Breeding age, female (years)
4.2
0.06
3
6
Breeding age, male (years)
4.88
0.06
4
6
Mating season (months) Overall pregnancy rate (%)
6.17 82.64
0.19 1.49
3 35.7
9 100
Pregnancy duration (months)
12.29
0.04
12
13
Mating after calving (months) Weaning age (months)
7.89 8.96
0.35 0.22
3 3
12 12
Calving interval (months)
22.73
0.47
15
36
3 months of parturition. The overall pregnancy rate was approximately similar in females bred early after parturition (≤ 3 months) and in those bred later (> 3 months). The mean calving interval was shorter (p = 0.008) in camels mated within 3 months of parturition (15.25 ± 2.8 months) than in those mated after that time (24.33 ± 6.5 months). The H/C significantly influenced the overall pregnancy rate (p = 0.003). Camel herds with H/C of 1:< 25 had higher overall pregnancy rate (95.29%) than herds with H/C of 1:25–50 (79.84%) and those with H/C of 1:> 50 (72.79%). The ME affected significantly the overall pregnancy rate (p = 0.001). Herds having ME of > 10 years revealed greater overall pregnancy rate (94.89%) than herds with ME of 5– 10 years (80.54%) and those with ME of < 5 years (72.5%). There were significant interactions between H/C × HS (p = 0.003), H/C × HS (p = 0.006), and ME × HS (p = 0.02). Other investigated parameters and their interactions had no influence on the overall pregnancy rate. Clinical endometritis, ovarian hydrobursitis, and vaginal adhesions were the common clinical findings of the barren females (Table 2).
Discussion According to the present study, herder/camels ratio (H/C) and manager experience (ME) are important factors affecting the reproductive performance in camel herds in Saudi Arabia. Herd size (HZ) and housing system (HS) might also influence the overall pregnancy rate through their interactions with H/C and ME. A camel manager duty often includes schedule herders work, address herders concerns, and oversee the day to day activities on the herd. Continuously training managers on the right and modern techniques of camel herd management is important to improve their administrative performance. Herders should be familiar with signs of estrus on females, determining the proper time for breeding and providing their help during the mating process to prevent unnecessary services or females at risk during mating by a vicious rut male. Their job necessitates a good knowledge of the signs of reproductive illness and prompt gynecological consultation.
The earlier veterinary intervention in treating infertility might affect the different indices of reproductive performance which explain the significant role of herders in improving the productivity of the camel herd. Data revealed that female dromedary camels can be bred efficiently as early as 3 years old, but most farmers withhold female camels from breeding until they are aged 4 to 5 years. Basically, pubertal timing is influenced by complex interactions among genetic, nutritional, environmental, and economic factors (Schillo et al. 1992; Abreu et al. 2015; Perry 2016). Puberty in dromedary camels commonly occurs at 3 to 4 years of age (Iwema 1960; Matharu 1966; Yagil 1985). The relatively older age at puberty in female dromedary camels can be due to the slow rate of growth. However, under improved conditions of nutrition and management, female camels have been able to achieve a body weight of 400 kg at 2 years and 513 kg at 3 years (Al-Metiery and AI-Hashemy 1986). On the other hand, in Kenya, under traditional nomadic management, camels reach their mature body weight between 7 and8 years of age (Schwartz et al. 1983). An attempt to accelerate the time of puberty has been practiced by Yagil (1985), whereby female camels (1.5 to 2 years of age) were injected with a synthetic FSH preparation (1000 units on three consecutive days). A year later, normal, healthy calves were born after normal parturition. However, breeding female camels before they reach 70% of their adult weight can increase the rate of abortion (Molash 1990).
Table 2
Clinical findings in barren female dromedary camels (n = 886)
Clinical findings
Frequency
Percentages (%)
Clinical endometritis Ovarian hydrobursitis Vaginal/cervical adhesion Overgrown follicles Hydro-/pyometra Ovarian inactivity Hydro-/pyoslapinx Apparently normal genitalia
388 325 65 50 25 13 11 9
43.8 36.7 7.3 5.6 2.8 1.5 1.3 1
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The male camels in this study reached breeding age slightly later than the females. According to Arthur et al. (1985); male camels display sexual activity at 2 years, but are not usually used as stud males until the age of five. One of the improper management practices observed in most herds in this study was the use of the males throughout their mating lifetime, while only a few herds replaced the stud male every 5 years. Using a large number of young bulls for a limited, short time is a solution for both maximizing the genetic trend and at the same time reducing inbreeding tendencies (Boichard et al. 2015). As observed in this study, the male/female ratio did not influence the reproductive efficiency in the camel herds. Based on the observation of Arthur et al. (1985), one male is sufficient for a herd of 200 females, but a smaller number of females are usually used because the breeding is intense over a relatively short breeding time. Based on the present data, dromedary camels in Saudi Arabia reproduce mainly in cooler weather, with pronounced sexual inactivity during the warm season. Farmers also prefer the cooler weather because they believe that the winter season is much better for the health of the calves. Factors that could affect the commencement of the breeding season in dromedary camels and its duration and intensity include local climatic conditions, length of daytime, rainfall, nutrition, presence of females and males in the same herd, and management (Bono et al. 1989; Merkt et al. 1990; Musa et al. 1993; Wilson 1984). Seasonality was more pronounced in the males than in the females. For females, during hot weather, the ovaries were inactive or showed a limited number of small follicles with irregular or extended follicular wave patterns (Musa and Abusineina 1978). In the United Arab Emirates, observations have indicated that well-fed and watered females showed limited ovarian activity throughout the summer; however, the determinant factors of the observed seasonality in conception rates were due to a decrease in libido in the male as environmental temperatures increased and to an increase in early embryonic death during the hot summer months (Skidmore 2011). For males, factors that have been reported include seasonal variation in testicular weight and activity (Abdel-Raouf et al. 1975), number of spermatozoa in the epididymis (Derar et al. 2005), structures and the histochemical content of the male accessory glands (Youssef et al. 1984), the levels of fructose and citric acid in different parts of the male genital organs (Badawy and Youssef 1982), the circulating testosterone levels (Derar et al. 2005), and the activity of the anterior pituitary gland (Hemeida et al. 1985; Ismail et al. 1985). Melatonin implantation during the non-breeding season has improved the libido and the reproductive performance of male dromedaries (Swelum et al. 2016), suggesting a role of melatonin in the seasonality of camels. The overall pregnancy rate observed in this study was relatively high, but it is similar to the findings of Arthur et al.
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(1985), who reported that of every 100 females mated in a particular season, 80 to 90 bore calves. On the other hand, lower calving rates of 28–57% have been reported in Tunisia (Djellouli and Saint-Martin 1992) and Kenya (Schwartz et al. 1983). The low fertility rates reported by various researchers could be partly related to parasitic and infectious diseases, as well as to managemental and nutritional factors (Ali et al. 2015; Bakheit et al. 2016; Tibary et al. 2006). A major weakness in the reproductive efficacy chain in dromedary camels is the long calving interval due to the prevalent practice of withholding the first postpartum mating for about 9 months after parturition. However, this problem is solvable because it is more about managemental matters than about animal physiology. In a study on the postpartum period in camels, involution of the uterus was completed by the fifthweek postpartum and ovarian activity resumed between days 14 and 17 postpartum. These camels were highly responsive to early GnRH treatment, and they could be mated between the fifth and sixth week after parturition with encouraging conception rates (Derar et al. 2014). Moreover, it was reported that four out of nine dromedary camels conceived between days 34 and 70 postpartum after hCG treatment (Vyas and Sahani 2000). According to herd managers, delayed mating of camels after calving is due to their desire to obtain more milk, to preserve the health of the mother and the newborn, and sometimes they are enforced to delay breeding if the birth is in the last season of mating. Adjusting the parturition to be at the beginning of the breeding season is an important step in this strategy in order to give the female a chance to get pregnant in the same breeding season and to avoid producing calves in the summer of the next season. Based on the present data, clinical endometritis, ovarian hydrobursitis, and vaginal adhesions are the main clinical findings of the barren female dromedaries in camel herds. Unhygienic gynecologic manipulation, unsanitary measures during parturition, and postpartum disorders are contributing factors for uterine infections (Wernery and Kumar 1994; Tibary et al. 2006). Ovarian hydrobursitis is a serious, longstanding, reproductive disorder in dromedary camels characterized by fluid accumulation and encapsulation of the ovary (Tibary and Anouassi 2001; Ali et al. 2011a, b; Benaissa et al. 2014). Many observations have suggested that ovarian hydrobursitis is originally an inflammatory procedure of the genital tract ([Ali et al. 2011a, b). It appears that Chlamydophila abortus is accountable for the distribution of the ovarian hydrobursitis infection in dromedaries (Ali et al. 2012). Chlamydophila could be transmitted by all methods of infection including the venereal route (Obendorf and Handasyde 1990; Higgins et al. 2005; Faber et al. 2011). Vaginal adhesion is a problem which threatens the reproductive life of female dromedary camels, as most of the female prevented from breeding because of occlusion of the genital tract. Injuries during parturition, chronic vaginitis,
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overbreeding, violent mating practices, and increasing parity could be suggested as reasons which contribute to the problem (Derar et al. 2015). Furthermore, some farmers place uncommon materials such as black seeds (Nigella sativa), dates, and salt in the vagina of camels with fertility problems as a part of ethnoveterinary practice. These materials may be infuriating to the mucus membrane of the vagina, prompting to vaginal and cervical adhesions.
Conclusion The continuing use of traditional systems of camel reproductive management hinders the opportunity to improve their reproductive efficiency. Improving the performance of managers and the ideal use of herders are important factors in maintaining high reproductive efficiency in camel herds. Reduction of age at first mating and the interval after calving can, however, be accomplished. Control of reproductive disorders and changing the strategy of using the stud males could also improve the quality of camel herds. These data are expected to be of considerable value to researchers, camel farmers, and those who, by extension, seek improvements in the welfare and productivity of the camel.
Compliance with ethical standards This study was approved by the Animal Care and Welfare Committee, Deanship of Scientific Research, Qassim University, Kingdom of Saudi Arabia. Conflict of interest The authors declare that they have no conflict of interest.
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