An Overview of the Reproductive Performance

Summary

Yaks are seasonal breeders with mating and conception constrained to the temperate season of the year. Usually, yaks are mated for the first time when they are 3 to 4 years old and are most likely to calve once every 2 years or twice in 3 years, producing 4 - 5 calves in a lifetime. Seasonal and general environmental conditions affect the reproductive rates rather markedly. The behavioral changes of estrus are not usually as clear as in other domestic cattle. The average length of the estrous cycle is approximately 20 days with the duration of estrus less than a day. Gestation length is around 258 days, shorter than in other cattle breeds. Abortion and other causes of premature termination of pregnancy are between 5 and 10%, however, the percentage rises with interspecies hybridization. Bulls usually start to mate at 3 or 4 years of age, they first have to establish a dominant position in the mating hierarchy of the herd and reach the peak of the mating ability around the age of 6 - 7 years. There is sufficient evidence to suggest that the reproductive rate of yaks can increase with improvements in a variety of management techniques geared to increase estrus frequency and conception rates.

Introduction

Yaks are one of the most remarkable domestic herbivores living on the Qinghai-Tibetan plateau, the "roof of the world". The plateau itself extends over 2.5 million sq km [1] as the most widespread high elevation region on earth and the best grasslands in Asia. From the core distribution area, yaks have also spread to the adjacent territories above the tree line where there are nearly no crops and there is not an absolutely frost-free period. Some 14 million yaks live and provide food, transport, shelter and fuel where few other animals will survive. It is quite possible that without the existence of the yak living in such harsh conditions, human civilization might not have reached and flourished in these remote areas.

Knowledge of the basic reproductive biology of yaks is necessary in order to improve the production potential of the animal. However, the number of publications relating specifically to yak reproduction is insignificant compared to other domestic species. The great majority of reports have been published as abstracts, short communications or theses and in many instance, the number of observations has been low. This review aims to document the reproductive performance of the yak under various sets of circumstances. Consideration will also be given to components of the reproductive process, in order to indicate which of these is the most limiting, or most amenable to change in the yak.

Reproductive Anatomy

The structure of the reproductive organs of the female yak differs in some aspects from those of dairy cows. The cervix in yaks has three transverse circles consisting of many tight folds, the average length of the cervix is 5.0+/- 0.9 cm long and the average external diameter is 3.2+/- 0.7 cm. The corpus uteri is rather short, being 2.1+/- 0.8 cm only. A long and distinct septum (approx 6 cm long) extends downward from the bifurcation of the uterine horn towards the uterine body. Because of the short uterine body and the long septum it is easy to deposit the semen in an optimal position such as the uterine body, uterine horn or the tips of the horn, especially since the cervix is relatively free within the pelvic cavity and can be readily held [2]. The ovaries in the yak are smaller than in dairy cows, the left ovary is 2.1 - 2.5 cm in length, 1.1 - 1 cm in surface to surface distance and 0.8 - 1.2 cm from attached to free border and the reported weight is 1.4 - 4.0 g. For the right ovary 1.8 - 2.4 cm in length, 1.2 - 4.8 cm in surface to surface distance, and 0.7 - 1.2 cm from attached to free border and the reported weight is 1 - 4.1 g. The length of the uterine tube is 18 - 24 cm [3-4].

Breeding Seasonality

Yaks are considered seasonal breeders. However, information about the breeding season is rather conflicting. The onset and the end of the breeding season are affected by ecological factors such as climate, grass growth, latitude and altitude. When temperature and humidity start to rise, grass starts to grow, body condition of yaks is improved following their long period of deprivation and weight loss over the winter, and females come into the breeding season. On the northwestern grasslands of Sichuan the season begins around June [5], at the higher elevation of Laqu in Tibet the breeding season will not start until July. Similar observations are reported from Kirgizia where the annual onset of the breeding season started on May 25th at an elevation of 1400 m and occur progressively later until at the altitude of 2700 m estrus started after June 22nd [6]. The breeding season reaches its peak in July and August when temperature is at its highest and grass growth is at its best. Thereafter, estrus frequency decreases and stops around November. Two examples from Qinghai, China and Mongolia are presented in Figure 1 [7-8]. Semen quality and quantity also change with season. The highest values for volume, sperm concentration and motility were obtained from June to September, with the peak occurring in September in Dangxi, Tibet [9].

Figure 1. Distribution of estrus in different months of the year.

Puberty

First estrus in yaks generally occurs in the second or third summer and autumn following birth, i.e., between 13 and 30 months of age. In Mongolia, around 10% of yaks come into the first estrus in the second summer of their life and most females do not show estrus until their third summer when they are more than 2 years old. Onset of first estrus is determined more by the body condition at the beginning of the breeding season than by age [10]. Very similar results based on observations on yak in Tuva Autonomous Republic were also reported [11].

In China, the majority of yaks are mated for the first time at the age of 3 years, i.e., in the 4th warm season following birth, but under favorable conditions some yaks may be mated a year earlier. Such conditions prevailed among 197 primaparous Jiulong yaks in the Sichuan province studied: 32.5% calved at 3 years, 59.9% at 4, 6.1% at 5, and the remaining 1.5% at 6 years or age. At these ages, yaks had reached between 75% and 100% of their mature weight [12]. In this context, yaks in Tuva reached fertile estrus at approximately 90% of mature body weight compared with 60% for Bos taurus cattle in that region [11]. First mating at the age of 2 years, though it also occurs in China, is more common among yaks in some other countries.

Males start to show mounting behavior around the age of 6 months. This behavior continues and intensifies to include searching and mounting females in the following year. No sperm, however, are found in epididymal fluid of yak bulls before the age of 2 years. Puberty thus occurs in the third warm season following birth, when the males are over 2 years old. In practice, bulls start to mate from the age of 3, reaching their peak ability at around 6 - 7 years old after establishing their dominant position in the mating hierarchy by fighting in the same herd (Fig. 2). After the age of 8, yak bulls start to lose to younger bulls in the competition for females [9].

Figure 2. Two male yaks fighting to establish their dominant position in the mating hierarchy of the herd.

A sexually productive life expectancy of not more than 10 years for a yak bull was indicated from results of an artificial insemination (AI) stud farm of 38 yak bulls in Tibet (elevation 4300 m). The ejaculate volume, concentration and motility of sperm rose steadily from the age of 3 to 9 years old and then declined [9].

In Mongolian yaks, the older the bull the more females it was able to serve, which was consistent with the courtship behavior and dominance hierarchy of bulls. However, it was also found that the younger bulls, with fewer females at their disposal, mounted their mates more frequently [10]. Fertilization seemed to be more dependent on the number of services than on the age of the bull, which showed that overall pregnancy rate of females increased with the number of services.

Estrus

The average length of estrous cycle in yaks has been reported to be 18 - 22 days (Table 1) and a great variation in the length is one of the problems in yak reproduction. The main reasons could be silent or non-detected estrus, delayed ovulation, implantation failure, or embryonic death. Estrus in yaks is greatly affected by the environment, and when the weather is unfavorable the onset of estrus is delayed, and when in favorable circumstances the onset of estrus in female yaks is advanced.

The duration of the estrus is not easily determined in the yak since the signs of estrus are not always clear. Estimates from northwestern Sichun suggest that estrus lasts 12 - 16 hours. In a study with 41 female yaks, 26 of them had an estrus lasting 24 hours or less and 4 yaks showed estrus for up to 72 hours. More than 80% of these animals ovulated within 24 hours after the end of estrus [16]. There is a tendency for the proportion of yaks with heat periods of 1 - 2 days to increase later in the breeding season when ambiant temperature begins to decline. Purevzav and Beshlebnov [17] recorded that among 54 Mongolian yaks, 26 were recorded on heat for only 0.5 to 6.5 hours, a further 17 females showed estrus between 6.5 and 12.5 hours, 7 females showed estrus between 12.5 and 18.5 hours, and only 4 females showed a longer estrus duration. Most of the yaks ovulate 12 - 24 hours after the end of estrus (10 out of 41, 24.4%) and some in 24 - 36 hours (2 out of 41, 4.9%) [16].

Changes in the appearance of the reproductive organs are more obvious than behavioral changes [21-22]. The vulva becomes swollen and the vagina reddens. Mucus is discharged from the vulva in a majority of females in estrus, but a substantial minority shows no such discharge; vagina and cervix dilate, the female tends to raise her tail and urinates frequently. As in other cattle, yak females on heat search out and ride other females and like to be approached by male yaks. However, these signs are less pronounced than in Bos tauruscattle. The most pronounced signs of estrus are following and mounting by mature bulls, swollen vulva, reddening of vaginal mucosa and mucous discharge.

Most yaks start to show estrus in the early morning or in the evening and only rarely at other times of day. Among 633 female yaks observed by Cai, two-thirds of the animals started to show heat before 9:00 hours when they had started grazing, and most of the remaining third started after 19:00 hours when grazing had ended for the day [21]. Similar observations were reported by Lei et al., [19]. Magash [10], however, with records for 73 yaks in Mongolia, found that only 38% came in heat between 2:00 and 8:00 hours, and 34% between 16:00 and 22:00 hours.

The average duration of postpartum anestrous at Xiandong farm in Sichuan Province was found to be 125 days, that figure, however, was subject to much variation [21]. Postpartum anestrous period was found to be much shorter (70.5+/- 18.5 days) for yaks in good body condition than for those in poor body condition (122.3+/- 11.8 days) [13]. The anestrous period following calving has been reported to be related to month of calving: 131, 124, 90 and 75 days for females calving in March, April, May and June, respectively, and 134, 130, 105, 89 and 37 days for each month from March to August [19].

Magasch [8] provided results on the interval between calving and first postpartum estrus for yak females in Mongolia, showing clearly a relationship with month of calving, the earlier the calving the longer the interval. However, there was considerable variation in these results around the average interval periods. Magasch reported that the service period following calving showed a very similar seasonal pattern for the interval between calving and first postpartum estrus.

The proportion of females that come into estrus in any one season depends on the previous calving history as well as on their body condition. Yaks can be divided into 3 categories: Those that calved in the current year and are lactating and nursing a calf (full lactating cow); those that calved in the previous year and are not pregnant, but may or may not be still nursing their calves ("Yama" or "half-lactating yak"), and those that previously had a calf, but not for at least 2 years and are not lactating ("Ganba"). In a study Yong et al., showed that from June to mid-September "Yama" had the highest proportion of females in estrus (112/161), "Ganba" came next (217/408) and full-lactating cows the lowest proportion 90/629 [23]. The three types of cows differ in pregnancy rate and the age of the females - with 5 - 6-years-old females having the best rate. By the age of 9 - 10 years the conception rate starts to decrease. In ordinary production herds in the mountainous regions of China, in general 50 - 70% of yak cows of suitable age show estrus in any one year, and that such yak females are mated and calve twice in 3 years or once every two years. In the absence of pregnancy, the number of individual estrus periods a female yak will experience in a breeding season can vary. It may also be affected by local environmental conditions and production system, including differences in temperature, nutrition and milking frequency. In some production systems, there are reports of yak females capable of showing estrus up to 3 to 4 times in the same season [21], including results reported for yak in the Tuva Republic [11] and in Mongolia [8].

Pregnancy and Parturition

Conception following mating at first estrus during breeding season is generally high. Among 68 females on heat, 53 had well-developed follicles and 15 did not probably due to uterine infections [21]. In a trail with 265 yaks that had previously calved, 72.4% became pregnant following the first estrus, a further 23.4% following the second, and 3.4% and 0.8% following the third and fourth cycles respectively [24]. In a similar investigation with 342 yaks in Mongolia, it was found that 70.5% were pregnant after the first service, 19.3% conceived to a second service and 4.6% to a third service, giving an overall pregnancy rate of 94.4% [8]. It appears from the above results that Mongolian yaks which are not pregnant at first-service, are able to return to estrus up to three times in the same breeding season.

In one particularly well-maintained herd of yaks on grassland in Gansu, where yaks had received some supplementary feed in late winter and early spring, a conception rate of 93.4% was achieved [16]. A pregnancy rate of 74.9% following insemination of 621 yaks with frozen semen at first estrus during the breeding season has also been reported [21].

Many studies have shown that it is not uncommon to achieve pregnancy rates above 70% either by natural service or by AI [15,25-26]. A survey showed that pregnancy rates depend much on the production system, and have ranged from 40% of 29760 yaks to 82+/- 6.2% of 8448 yaks [20]. However, pregnancy rates are markedly reduced for pregnancies resulting from inter-species cross-breeding when compared to pure-breed matings. When female yaks are inseminated with semen (or mated by a bull) of other species of cattle, incompatibilities appear to arise and pregnancy rates decrease. The gestation length of yak is shorter than that of Bos taurus, particularly when a pure yak calf is carried. Yaks carrying a pure-breed calf usually have a shorter gestation length than when carrying an inter-species crossbred calf. The average gestation length of yaks with a crossbred calf, the Pian Niu (yak x cattle hybrids) was found to be around 270 days (273.2 days with a SD of 12.7 days for 371 cows carrying male F1 calves and 268.7 days with a SD of 10.2 days for cows carrying female F1 calves ) [25]. For yaks with purebred calves, Denisov reported an average gestation length of 258 days [6]; Lei et al., recorded a gestation length of 260 days for 36 yaks (253 - 278 days) for those carrying male calves and 250 days (226 - 283 days) for those carrying female calves [19]. Dubrovin recorded an average gestation length of 258 days for 800 yaks in the Caucasus [27]; Katzina and Malturova recorded a gestation length of 259 days (228 - 280 days) for yaks in the Tuva region [11], and Yu et al., reported an average of 254 days ( 248 - 258 days, SD 2.7 days) for yaks in Gansu [16]. Joshi et al., reported an average gestation length of 258 days in Nepal [26].

Almost all births take place during the day and only very few at night when yak cows are normally at the herders’ campsite. When the time for parturition approaches, the female looks for a sheltered spot, such as a depression in the ground or ditch, at a distance from the herd. Typical behavior of the yak during labor includes lying on her side and standing up again for delivery. Dystocia is a rare occurrence in yak with purebred calves. The umbilical cord is severed by mechanical stretching as the cow gets up or the calf falls down after delivery. Yak cows with hybrid calves, however, require help for delivery. For example, there were 28 cases of dystocia among 681 such calvings (4.1%) over a period of 10 years in one study in Sichuan [4]. Twins are rare, and represent only about 0.5% of all births, but in exceptional breeds higher rates have been recorded [21]. The dam generally licks the newborn calf for about 10 mins after which the calf attempts to stand up and suck. Again, differences in behavior have been observed between dams delivering purebred yak calves and Pian Niu calves (Table 2) [29], with some time intervals markedly longer when a Pian Niu calf is involved rather than when pure yak calves are born.

Ganbat & Magash [34] recorded the course of parturition in yak cows. The dilatation of uterine cervix lasted 228+/- 22.2 min, the period of expelling fetus lasted 25.2+/- 2.6 min and the placenta expulsion lasted 136+/- 0.5 min. The total process of parturition lasted 339.2 min [33].

The placenta is passed within half an hour and up to 6 hours after parturition. In the period shortly after birth, the dam is intensely protective of her calf and will attack any person coming close. Bonding between dam and calf depends mainly on smelling and licking. Longer parturition times and dystocia militate against such bonding and thus place Pian Niu calves at a disadvantage versus purebred yak calves.

The calving season in Mongolia is extended over a few months. It can be estimated that a small proportion of yak cows calved in March, probably around 25% in April, many more in May (the peak month), and a declining number in June and July [8]. Denisov reported from Kirgizia that the calving season for a herd of 597 yaks extended from February to December. However, only 5 calves were born in February, and 116 (19.4%), 253 (42.4%) and 113 (18.92%) respectively over the next 3 months and tailing off rapidly thereafter [6].

When yaks are cross-bred to produce Pian Niu animals, it is common to attempt hybridization either by natural mating or AI in the first half of the breeding season followed by the use of yak bulls to catch cows that have not conceived and have returned to estrus. Thus, it is not uncommon for crossbred calves to be born earlier than purebred calves.

Abortion and other causes of premature termination of pregnancies account for 5 - 10% of all pregnancies, as observed in 971 yak females in Laqu, Tibet with an abortion rate of 5.7% [21]. Calving rate is lower when interspecies hybridization is involved. Among 1438 female yaks carrying crossbred calves in north-western Sichuan, 20% lost their calves, and in another study with 158 young pregnant females, 14 lost their crossbred calves before normal parturition [23].

A 90% survival rate is typical among purebred calves (1328/1470) among Jiulong yaks in Sichuan [30], and 89.8% (1818/2025) for purebred calves at Datong Farm, Qinghai [31]. In contrast to the greater problems experienced before and during parturition with Pian Niu calves, crossbred calves, once delivered, have a slightly better survival rate than pure yak calves. Results at the same locations stated above, showed survival rates for Pian Niu calves to be about 2% better.

Detailed observations [32] of 20 yak calves on a farm at an elevation of 3500 - 4100 m showed that neonatal survival was also related to the maintenance of body temperature in the calf. The fall in body temperature in the first hour after birth (average fall 0.38oC) was significantly correlated (r = 0.69) with birth weight (the greater the weight, the lower the temperature loss), and much less strongly correlated with ambient temperatures. Thus the body condition of the dam during pregnancy affects calf survival through its effect on birth weight. The body temperature of the calves returned to normal after 3 hours.

Exceptional yak females may live to an age of about 24 years, but 15 - 16 years is the normal upper limit for reproductive activity. The peak reproductive ability is considered to be between the 5th and the 9th year of life [32].

Yu and Chen studied a total of 1953 yak cows (3 - 11 years of age) in two populations differing in calving rates. The calving rate was 78% in the high calving rate group and 50% in the other [34]. It appears that the main differences are due to milking frequency and feed supplementation between the two populations. The high calving rate group was milked once daily and received supplementary feed from late winter to early spring, whilst the low calving rate group was milked twice daily and did not received any supplementary feed.

Calving interval is an important economic index in the yak industry. Wang et al., [35] observed 439 calvings from 161 yaks over a 7 year period. The average calving interval was 459+/- 131 days, showed a tendency for gradual decrease with increase in parity.