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Reproductive cycles of buffalo

Department of Farm Animal Production and Health, Faculty of Veterinary Medicine & Animal Science, University of Peradeniya, Peradeniya, Sri Lanka The domestic water buffalo (Bubalus bubalis) has an important role in the agricultural econ- omy of many developing countries in Asia, providing milk, meat and draught power. It isalso used in some Mediterranean and Latin American countries as a source of milk and meat for specialized markets. Although the buffalo can adapt to harsh environments and live poor quality forage, reproductive efficiency is often compromised by such conditions, resulting in late sexual maturity, long postpartum anoestrus, poor expression of oestrus, poor conception rates and long calving intervals. The age at puberty is influenced by geno- type, nutrition, management and climate, and under favourable conditions occurs at 15–18months in river buffalo and 21–24 months in swamp buffalo. The ovaries are smaller than incattle and contain fewer primordial follicles. Buffalo are capable of breeding throughout theyear, but in many countries a seasonal pattern of ovarian activity occurs. This is attributed intropical regions to changes in rainfall resulting in feed availability or to temperature stressresulting in elevated prolactin secretion, and in temperate regions to changes in photope-riod and melatonin secretion. The mean length of the oestrous cycle is 21 days, with greatervariation than observed in cattle. The signs of oestrus in buffalo are less overt than in cattleand homosexual behaviour between females is rare. The duration of oestrus is 5–27 h, withovulation occurring 24–48 h (mean 34 h) after the onset of oestrus. The hormonal changesoccurring in peripheral circulation are similar to those observed in cattle, but the peak con-centrations of progesterone and oestradiol-17␤ are less. The number of follicular wavesduring an oestrous cycle varies from one to three and influences the length of the lutealphase as well as the inter-ovulatory interval. Under optimal conditions, dairy types man-aged with limited or no suckling resume oestrus cyclicity by 30–60 days after calving, whileswamp types with free suckling do so at 60–90 days. However, in many farming systemsprolonged postpartum anoestrus is a major problem, and the causes include poor nutritionand body condition, and stress due to harsh climates and improper management. Synchro-nization of time or induction of oestrus can be done using the same regimens as applied incattle, using various combinations of prostaglandins, progesterone releasing devices, GnRHand eCG, but success rate is poor when treatment is done during the periods of marginalbreeding activity or seasonal anoestrus.
2010 Elsevier B.V. All rights reserved.
1. Introduction
The domestic water buffalo (Bubalus bubalis) is an important livestock resource in many countries of Asia,the Mediterranean region and Latin America. The world ଝ This paper is part of the special issue entitled: Reproductive Cycles of population of buffalo is estimated to be 172 million (FAO: Animals, Guest Edited by Michael G. Diskin and Alexander Evans.
falo are classified in to two main ‘types’: the river type 0378-4320/$ – see front matter 2010 Elsevier B.V. All rights reserved.
doi: B.M.A.O. Perera / Animal Reproduction Science 124 (2011) 194–199 located in South Asia and the swamp type spread across systems. In Europe, buffalo of the Mediterranean type pre- dominate and are kept on large commercial farms under ranean buffalo, which some consider to be a third type, is modern intensive systems for milk and meat production. In derived from the river type. The main breeds of dairy buf- the Latin American region river, swamp and cross-bred buf- falo belong to the river type and include the Murrah, Surti, falo are produced, with production systems varying from Jafarabadi and Nili-Ravi. The swamp type has no special- extensive beef production, through dual-purpose systems ized breeds but selective breeding in some countries has to intensively managed herds for milk production.
resulted in populations with characteristic features.
The buffalo has been traditionally regarded as a poor 1.2. Previous reviews on buffalo reproduction breeder due to having poor fertility in the majority of con-ditions under which they are raised ( The reproductive physiology and endocrinology of domestic buffalo and the comparative aspects with cat- rity, long postpartum anoestrous intervals, poor expression of oestrus, poor conception rates (CR) and long calving intervals. However, studies in Sri Lanka ( those relating to the application of reproductive technolo- that fertility can be highly acceptable, provided genotypes and More recently, a collection of papers are matched to the environment and the animals are man- containing in-depth reviews on several aspects of repro- duction and production was published by FAO and the current status of knowledge on reproduc- 1.1. Role of the buffalo in livestock production in tion and reproductive technologies was summarized by present review dealswith the normal reproductive cycle of the buffalo, with Systems of buffalo production vary widely through the emphasis on some unique features in this species, and a brief overview of methods for controlling the reproductive and are determined by several interacting fac- tors that include climate (tropical or temperate, humid orarid), location (rural, peri-urban or urban), cropping sys- 2. Puberty and the mature reproductive organs
tems (rain-fed or irrigated, annual or perennial crops), typeof operation (small or large farm, subsistence or commer- cial), and primary purpose for buffalo production and/ormanagement (milk, meat, draught or mixed).
Buffalo heifers usually attain puberty when they reach In South Asia, buffalo are predominantly of the river about 55–60% of their adult body weight, but the age at type and produced mainly for milk and meat production which they attain puberty can be highly variable, ranging by small-holders in subsistence or semi-commercial farms.
Intensive systems of management are practiced in irrigated factors that influence this are genotype, nutrition, man- and rain-fed cropping areas, while extensive systems are agement, social environment, climate, year or season of common in semi-arid and arid regions where free grazing birth and diseases. A review of studies from many countries is available on communal lands. The latter systems often include use of buffalo as draught animals. Peri-urban sys- river type buffalo exhibit first oestrus at 15–18 months of tems are found around major cities, where large herds are age, while the swamp type do so at 21–24 months. The body raised purely for milk production under intensive condi- weight at which puberty is attained is strongly influenced tions, with cows having greater production yielding 15–20 l by genotype and is around 200–300 kg for the swamp type of milk per day at peak lactation being brought in from and 250–400 kg for the river type. Although buffalo attain other areas soon after calving, and disposed after 200–300 puberty later than cattle, they have a longer reproductive days, when the yield drops to an uneconomical amounts.
life, which tends to compensate for this early economic In East and South-East Asia, the swamp type predom- inates and is reared mainly for draught power and meat,on small farms with integrated crop-livestock farming sys- 2.2. Ovaries, follicles and corpora lutea tems. The buffalo also serves as a capital asset to protectagainst economic risks such as crop failure, and features The ovaries of post-pubertal buffalo heifers have a reser- in religious and cultural events in some communities.
voir of only 10,000–20,000 primordial follicles ( The production systems are mostly extensive or semi- compared with over 100,000 in cattle. The mature intensive, with free or tethered grazing in home gardens, ovaries are smaller than in cattle, weighing around 2.5 g when inactive and 4 g when active, with fewer tertiary fol- The majority of buffalo in North Africa and the Middle East are of the river or Mediterranean type and are con- rectum, mature follicles in swamp buffalo rarely exceed centrated around the Nile delta. These animals are kept 8 mm in diameter, tend to protrude from the surface of mainly by small-holders for producing milk and eventu- the ovary and can be mistaken as an early developing cor- ally beef. A few commercial operations exist in urban areas, for specialized production of milk and beef under intensive is smaller than that in cattle, often does not protrude B.M.A.O. Perera / Animal Reproduction Science 124 (2011) 194–199 markedly from the surface of the ovary and sometimes adverse environmental conditions, nutrition and irregular- lacks a clear crown. These characteristics make accurate ities in secretion of ovarian steroid hormones ( identification of ovarian structures by rectal palpation in The duration of oestrus is similar in river and swamp Wishy, Ultrasonic imaging indicates mature follicles buffalo, varying between 5 and 27 h, and ovulation occurs range in size from 1.3 to 1.6 cm in diameter and mature cor- about 24–48 h (mean 34 h) after onset of oestrus, or 6–21 h pora lutea from 1.2 to 1.7 cm in diameter ( In hot climates duration of oestrus tends tobe shorter and signs of oestrus may be exhibited only dur- ing the night or early morning. In Italian buffalo differentdurations of oestrus have been observed The uterus and cervix of buffalo are smaller than those and categorized as short (<12 h), medium (13–24 h), long in cattle and the non-pregnant tract lies wholly within the (24–48 h) and very long (>48 h). In the short and medium pelvic cavity with the uterus usually being tightly coiled oestrous cycles ovulation occurred after the end of oestrus, around 6–72 h and 24–60 h after the onset of oestrus, in cattle and is more difficult to negotiate during artificial respectively. In some of the long and very long oestrous insemination (AI), especially in heifers.
cycles ovulation occurred before the end of oestrus.
3. Reproductive patterns and the influence of
4.2. Reproductive hormones and temporal relationships nutrition, ambient temperature and photoperiod
Buffalo are polyoestrous and are capable of breed- The changes in concentrations of progesterone in blood ing throughout the year. However, in many countries a and milk during the oestrous cycle are similar to those seasonal pattern of breeding activity, and consequently in cattle, but the peak concentration is relatively less calving, has been observed. In tropical locations where pho- toperiod is relatively constant, annual changes in rainfall Progesterone concentration in fat-free milk appear to influence oestrous cyclicity, with availability and is usually below 1 nmol/l (∼0.3 ng/ml) during the follic- quality of herbage related to this cyclical reproductive pat- ular phase of the oestrous cycle and ranges from 3 to tern. In the dry zone of Sri Lanka, buffalo kept under free 12 nmol/l (∼1–4 ng/ml) during the luteal phase and preg- grazing commence ovarian activity some 2–3 months after the onset of monsoonal rains, followed by conceptions that result in a peak calving season 10 months later ( ity and for early diagnosis of non-pregnancy, progesterone Similar effects of climate and nutrition on reproduc- concentrations above 3 nmol/l are considered to be indica- tive patterns have been observed in India tive of the presence of luteal function and those below 1 nmol/l are considered indicative of the absence of luteal Heat stress during the hot summer months in India is function, with intermediate values being considered incon- a major cause of anoestrus in buffalo and is associated with elevated blood concentrations of prolactin, which The concentration of oestradiol-17␤ in blood during the is thought to influence ovarian activity as well as cause follicular phase of the oestrous cycle also appears to be rel- sub-fertility and repeat breeding by decreasing proges- regions such as Italy, however, where buffalo are fed with been suggested as a possible reason for the lesser intensity a constant balanced diet, a distinct seasonal reproductive of oestrus exhibited by buffalos, studies on Italian buf- pattern is also found, and the inference from a series of falo have shown no differences in the endocrine profiles studies is that seasonality is influenced by photoperiod of those with overt and oestrus without an associated ovu- The effects of these and other factors on postpartum ovarian activity are discussed in Section gonadotrophic hormones in blood of buffalo indicate that the temporal patterns of both LH and FSH are basicallysimilar to those in cattle 4. Oestrous cycles
with a preovulatory LH surge occurring on the dayof oestrus and lasting 7–12 h. In Italian buffalo a significant 4.1. Duration and variability of the oestrous cycle and difference in the interval from peak concentration of LH to ovulation has been observed in animals that conceivedto AI and those that did not, being 25 ± 13 and 46 ± 18 h, The duration of the oestrous cycle in buffalo is similar to that in cattle, ranging from 17 to 26 days with a mean A study in which timing of oestrous cycles among Mur- there is greater variability of oestrous cycle length in buf- concentrations of LH and FSH of 38 and 24 ng/ml were falo, with a greater incidence of both abnormally short and detected, respectively, during oestrus. Concentrations of long oestrous cycles, attributed to various factors including FSH in the plasma showed three mid-cycle elevations B.M.A.O. Perera / Animal Reproduction Science 124 (2011) 194–199 For buffalo with two-waves of ovarian follicular develop-ment during oestrous cycles, the growth rate and diameterof the largest follicle was significantly smaller in heifersthan cows for both the first follicular wave (1.3 comparedto 1.7 mm per day and 10.5 compared to 13.3 mm, respec-tively) and the second follicular wave (1.0 compared to1.3 mm per day and 11.0 compared to 13.8 mm).
A recent study on suckled Thai swamp buffalo has shown that the first postpartum ovula-tion was followed by a short oestrous cycle (10.2 ± 0.38days) in 84% of the animals, but the prevalence of thesedecreased thereafter. The mean diameters of ovulatory fol- Fig. 1. Schematic representation of the hormonal changes occurring in
licles increased between the first and second ovulation blood of buffalo during the oestrous cycle.
(13.50 ± 0.52–14.31 ± 0.38 mm), and the mean diameter ofan ovulatory follicle and that of the resulting corpus luteum which corresponded to comparatively less inhibin and were significantly larger in those that became pregnant at elevated oestradiol-17␤ concentrations during the same that ovulation than in those that did not become pregnant.
period, leading to the conclusion that both inhibin and Further studies are clearly warranted to examine the rea- oestradiol-17␤ have a feed-back regulatory effect on FSH sons for the above differences, and to determine whether they influence the quality of the oocyte in the dominant A schematic representation of the hormonal changes follicle that is destined for ovulation.
occurring in blood of buffalo during the oestrous cycle,summarized from the literature reviewed above, is Externally detectable physical changes around the time 4.3. Waves of ovarian follicular development during the of oestrus include swelling of the vulva and reddening of the vestibular mucosa (Vulval swelling results in obliteration of the horizontal Ovarian follicular growth during the oestrous cycle in wrinkles which are present on its external surface and this, together with vestibular reddening, can be detected by basically similar to that in cattle, characterized by waves regular examination of individual animals under confined of follicular recruitment, growth and regression. How- systems. Mucus secreted from the cervix during oestrus is ever, interesting and as yet unexplained differences in the less copious than in cattle, does not usually hang as strands number of follicular waves per oestrous cycle and the char- from the vulva, but tends to accumulate on the floor of the acteristics of follicular growth and regression have been vagina and be discharged either when the animal is lying reported from buffalo in different countries.
Thus in buffalo that are housed or tethered, detec- showed that the number of follicular waves during tion of oestrus can be aided by examining the floor near the an oestrous cycle was one in 3% of animals, two in 63% rear of the animal each morning and evening for signs of and three in 33%. The first wave commenced on day 1 (day 0 = ovulation) in all categories of animals, while the sec-ond wave emerged on days 10.8 and 9.3 for the animals with 2 and 3 wave cycles, respectively, and the third waveemerged on day 16.8 in the latter group. The oestrous cycles A major difference between buffalo and cattle is that with two and three follicular waves of follicular develop- behavioural signs of oestrus are less overt than in the for- ment differed in the mean length of the luteal phase (10.4 mer, with homosexual behaviour between females being compared to 12.7 days) and the interval between ovula- tions (22.3 compared to 24.5 days). A study on Egyptian absence of a bull, the main behavioural signs are restless- buffalo, however, indicated the majority of oestrous cycles ness, bellowing and frequent voiding of small quantities of (54%) had three waves of follicular development urine, but these are not consistently exhibited by all ani- mals. When a bull is present, however, the bull will show Studies on Italian buffalo indicate differences in increasing interest in a cow that is approaching oestrus, ovarian follicular dynamics between nulliparous heifers and the cow will stand to be mounted by the bull during oestrus. During periods of greater ambient temperature the oestrous synchronization protocol using progesterone and duration of oestrus may be shorter and the oestrual signs prostaglandin, heifers exhibited one, two or three waves exhibited only during the night or early morning.
of ovarian follicular development during an oestrous cycle,with inter-oestrous intervals of 8–12, 20–26 and 25 days, 5. Postpartum reproductive events
respectively. In contrast, all parous cows had a two-wavesof ovarian follicular development during oestrous cycles As in cattle, uterine involution in buffalo is usually com- with an inter-oestrous interval ranging from 19 to 25 days.
B.M.A.O. Perera / Animal Reproduction Science 124 (2011) 194–199 have prompted studies aimed at manipulating follicular The period of postpartum anoestrus or anoestrus is usu- development to achieve greater oestrous synchrony and ally longer in buffalo than in cattle under comparative A review of studies using various treatment pro- falo resume anoestrus by 30–90 days, but factors such as prostaglandins either alone or in combination with GnRH ranged from 7 to 56%, while CR following the use of a pro- gesterone releasing devices either alone or in combination with eCG, and in some cases further supplemented with ence nutrition through feed quality and availability, can hCG or GnRH, ranged from 8 to 64%. The ‘Ovsynch’ protocol delay this considerably. For example, indigenous buffalo in (GnRH followed by prostaglandin 7 days later and a second Sri Lanka raised under free grazing with abundant natural GnRH 2 days later) has been used successfully in buffalo, feed and calves allowed access to the dams for suckling with synchronization of time of ovulation in 70–90% and CR only once per day, resumed oestrous cyclicity by 30–60 days after calving, whereas those under harsher conditions In most studies the success rate was lower when treat- with free suckling by the calves remained anoestrual for ment was done during the periods of low breeding activity or during seasonal anoestrus, and various modified pro- A review of the literature on postpartum anoestrus in tocols have been tried to overcome these problems. The two most effective approaches appear to be the Ovsynch of infertility resulting in economic loss to buffalo breeders protocol supplemented by administration of progesterone in many countries. In Egypt, India and Pakistan only 34–49% for 7 days between the first GnRH and prostaglandin treat- of animals showed oestrus during the first 90 days after ments, and progesterone based regimens of 10–14 days calving, while 31–40% remained anoestrous for more than with either GnRH or oestradiol treatment at the time of 150 days. The first postpartum ovulation was frequently progesterone implant insertion and prostaglandin plus eCG followed by one or more short oestrous cycles (<18 days) and cessation of oestrous cyclicity occurred after the first or second ovulation in about 25% of animals due to ovulatory In addition to the type of protocol selected, the follow- failure or prolonged luteal activity. In India, the incidence ing factors must also be addressed when using any regimen of postpartum anoestrus in buffalo herds can range from in buffalo ((a) selection of animals that are in 20 to 80%, with the greatest incidence during hot summers good body condition score and free from disease; (b) min- imize stress during the treatment administration and AI, LH secretion in buffalo remains low during the early especially under tropical conditions, when animals may be postpartum period and episodic pulses become detectable herded together, tethered or moved to other locations; and a few weeks before ovarian activity commences, with ani- (c) where seasonal differences exist, scheduling treatments mals that are subjected to better nutrition and restricted for the more favourable periods or during the peak of the suckling commencing episodic release of LH earlier than breeding season when the majority of animals are likely to those under poor nutrition or free suckling The response of LH secretion to a challenge of exoge-nous GnRH at 25–35 days postpartum, measured as peak Conflict of interest statement
concentration and area under the curve, is greater in non-suckled than suckled buffalo The author has no financial or personal relationship Methods that are recommended for overcoming pro- with other people or organisations that could inappropri- longed postpartum anoestrus in buffalo include adequate ately influence or bias the paper entitled “Reproductive nutrition before and after calving, restricting the suckling by calves and alleviating heat stress by permitting wal-lowing or use of water sprinklers Thepresence of buffalo bulls in a herd also has a biostimulatory References
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