www.elsevier.comrlocateranireprosci
The reproductive pattern and efficiency of female
buffaloes
J. Singh
a,), A.S. Nanda
b, G.P. Adams
ca
Department of Veterinary Anatomy, Punjab Agricultural UniÕersity Ludhiana, 141004 Punjab, India
b
Department of Animal Reproduction, Gynecology and Obstetrics, Punjab Agricultural UniÕersity Ludhiana,
141004 Punjab, India c
Department of Veterinary Anatomy, UniÕersity of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N 5B4
Abstract
Buffaloes play a prominent role in rural livestock production, particularly in Asia.
Reproduc-Ž .
tive efficiency is the primary factor affecting productivity and is hampered in female buffalo by i
Ž . Ž .
inherent late maturity, ii poor estrus expression in summer, iii distinct seasonal reproductive
Ž .
patterns, and iv prolonged intercalving intervals. Ovarian function is central to these issues; hence, the focal point of this review is ovarian function in Bubalus bubalis, particularly, in relation to seasonal changes. Ovarian anatomy, follicular and luteal development development, and hormonal profiles during the estrous cycle are discussed. Review of the literature revealed a paucity of critically derived information on follicular and ovulatory patterns in buffalo, particu-larly, in relation to seasonal estrusrbirthing. Efforts may be directed at understanding the process
Žrecruitment, development, atresia and temporal pattern follicle selection, dominance, subordi-. Ž .
nate follicle suppression, follicle numbers, and, preovulatory changes of follicular dynamics using techniques which permit serial assessment of changes occurring over time. Emphasis may be directed towards investigating follicular ‘‘waves’’ as a functional unit, rather than the estrous cycle, in the context of whole animal endocrinology. The data obtained from such basic studies may then be used to develop and test models for enhancing reproductive efficiency. q2000
Elsevier Science B.V. All rights reserved.
Keywords: Buffalo; Ovary; Reproduction; Reproductive efficiency; Reproductive patterns; Seasonality
)Corresponding author.
Ž .
E-mail address: [email protected] J. Singh .
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
Ž .
1. Introduction
Ž . Ž .
Among the African Syncerus coffer and Indian Bubalus spp. groups of buffaloes,
Ž .
only the Indian wild buffalo Bubalus arni has been domesticated and has been named Bubalus bubalis. Subspecies of B. bubalis are referred to as river buffalo and swamp buffalo. While river buffaloes are commonly found in the Indian subcontinent, Mediter-ranean region of Europe, South America and the Caribbean, swamp buffaloes are commonly seen in Southeast Asia and China. The river buffalo is a triple purpose species contributing milk, draft-work and meat, while the swamp buffalo is considered a dual-purpose species — draft and meat. Despite river and swamp buffalo possessing a
Ž .
different number of chromosomes 2 ns50 and 48, respectively , they are able to
Ž .
interbreed and produce fertile hybrid progeny Xiao, 1988 .
More than 50% of the estimated world population of 148 million buffaloes is in India
ŽAgarwal and Tomar, 1998 . Murrah, Nili-Ravi, Surti, Mehsana, Nagpuri and Bhadawari.
are the most common breeds. Buffaloes contribute 10% of the world’s total milk
Ž . Ž
production, virtually all of which )99% is produced in developing countries Shah,
.
1988 . Regarding meat production, an estimated 1.6 million metric tons of buffalo meat
Ž .
is produced annually Agarwal and Tomar, 1998 . As a beast of burden, the buffalo is considered the tractor of most of Southeast Asia, providing 20% to 30% of farm power in China, Thailand, Indonesia, Malaysia and the Philippines.
It is clear that buffaloes play a prominent role in rural livestock production, particularly in Asia, and factors affecting productivity are of paramount importance to agricultural economics in this region of the world. Reproductive efficiency is the
Ž .
primary factor affecting productivity and is hampered in female buffalo by i inherent
Ž . Ž .
late maturity, ii poor estrus expression in summer, iii distinct seasonal reproductive
Ž . Ž
patterns, and iv prolonged intercalving intervals Madan, 1988; Madan and Raina,
.
1984 . Hence, the focal point of this review is the form and function of the ovaries of B. bubalis, especially as they are affected by reproductive status and season.
2. Ovarian anatomy
The buffalo ovary is elongated and considerably smaller than that of cattle. The
average dimensions of the buffalo ovary vary between 22–26=11–18=11–14 mm3
ŽFadle et al., 1974 with a maximum and minimum weight of 6.1 and 2.9g, respectively.
ŽEl-Wishy et al., 1971 . The corpus luteum CL of the buffalo is often deeply embedded. Ž . Ž
in ovarian stroma and is generally smaller than that of cattle maximum weight 2.3 g,
.
maximum diameter 15 mm; Roy and Mullick, 1964 . Examination of excised ovaries
ŽDanell, 1987 revealed that the left–right distribution of ovulation as indicated by the. Ž .
3. Estrous cycle, estrus and ovulation
Although not compared critically, there appear to be considerable differences in reproductive traits among different breeds of buffaloes. The average length of the estrous cycle has been reported to be 20–22 days for river buffaloes; however, great
Ž
variations have been observed under rural conditions Agarwal and Purbey, 1983;
.
Madan, 1988 . The average duration of estrus appears to be slightly longer in river
Ž . Ž
buffalo 23.8"6.2 h; Danell, 1987 than in swamp buffalo 19.9"4.4 h; Kanai and
.
‘Shimizu, 1983; Shimizu, 1987 . A seasonal variation was reported in one study
ŽJanakiraman, 1978 wherein the duration of estrus was estimated to be 14, 18, and.
8–10 h in the monsoon, winter, and summer seasons, respectively, in river buffaloes.
Ž .
Salient signs of estrus in river buffalo Surti and Nili-Ravi breeds are decreased milk
Ž
yield, bellowing, vulvar swelling and mucus discharge Kamizi, 1983; Rao and
Koda-.
gali, 1983; Danell et al., 1984 . Swamp buffaloes exhibit a higher frequency of, and
Ž .
submission to, vulvar sniffing during estrus McCool et al., 1989 . The interval from the
Ž
end of estrus to ovulation has been estimated to be 11 h in Indian buffaloes nondescript
. Ž .
breeds, Luktuke and Ahuja, 1961 , 12–24 h in Surti buffaloes Danell, 1987 , 14.8"0.4
Ž . Ž
h in Nagpuri buffaoes Raut and Kadu, 1988 and 13.9 h in swamp buffaloes Kanai and
.
Shimizu, 1986 .
4. Follicle development
Ž .
Follicular development has not been studied in detail in buffalo. Left 49.3% and
Ž . Ž .
right 50.7% ovaries have a similar number of primordial follicles Danell, 1987 . The
Ž
population of primordial follicles was estimated to be 19,000 Samad and Nasseri,
. Ž .
1979 . In a more critical study Danell, 1987 , Surti buffaloes possessed 10,132
Žanestrus animals. to 12,636 Žcycling animals. primordial follicles. In cattle, the
estimated mean number of primordial follicles decreased from 133,000 at birth to less
Ž .
than 3000 at 20 years of age Erickson, 1966 . Although the number of primordial folicles appears to be considerably lower in buffaloes than in cattle, the effect of age on the population has apparently not be evaluated in buffaloes. In addition, buffalo ovaries
Ž
contain only about 20% of the number of antral follicles found in cattle ovaries 48
.
versus 233;Ty et al., 1989 . Cycling versus noncycling Surti buffalo heifer ovaries
possessed 46.3 versus 67.8 follicles )1 mm, and 16.8 versus 23.6 follicles )2 mm,
Ž .
respectively Danell, 1987 . The average number of follicles visible on surface of each
Ž .
ovary was 5.2"1.0 Kumar et al., 1997 . In Surti buffaloes, the average proportion of
Ž .
antral follicles that appeared to be atretic, histologically, was 71% Danell, 1987 ,
Ž .
compared to 82% 71.4% during follicular phase and 94.4% during luteal phase in
Ž .
swamp buffaloes Ocampo et al., 1994 . Evaluation of the number of follicles )2 mm
in ovaries excised at three different time periods of the estrous cycle revealed a greater
Ž .
number between Days 1–8 and 9–11 than during Days 12–21 Danell, 1987 . Large
Ž7–8 mm follicles could be palpated during Days 9 to 13 of the estrous cycle in 65% of.
Ž .
post-pubertal buffalo heifers Singh et al., 1984 . Phase-related differences in the
hypothesis that follicular development occurs in a wave-like pattern in buffaloes, similar to cattle. This hypothesis remains to be tested.
5. Hormonal profiles during estrous cycle
Reproductive endocrinology of the buffalo has received considerable attention during the last two decades. Although steroid hormone concentrations have been measured with reasonable accuracy, measurement of gonadatropins has been hindered by a lack of purified hormone preparations for antibody production and radio-iodination for develop-ment of homologous LH and FSH immunoassays. Moreover, lack of uniform standards among different laboratories poses another difficulty. Hence, the results of LH and FSH profiles should be interpreted with caution at this stage.
The basic pattern of changes in hormone profiles of buffaloes during the estrous cycle closely resembles that of cattle. The concentration of blood progesterone is at its nadir
Ž0.1–0.3 ngrml during estrus and remains close to 1 ng. rml for the next 3–4 days
ŽArora and Pandey, 1982 . The first significant increase in progesterone concentration.
Ž .
occurs about 7 days after estrus Ahmed et al., 1977 . Peak progesterone values of
Ž .
4.0–5.1 ngrml Bachlaus et al., 1979; Arora and Pandey, 1982; Takkar et al., 1983
have been recorded about 15 days after estrus. Circulating estradiol concentrations
Ž .
remain low during the luteal phase with minor fluctuations 10–20 pgrml around Days
Ž
4 and 10 of the estrous cycle in river buffalo Batra and Pandey, 1982; Samad et al.,
. Ž .
1988 , but not in swamp buffalo Kanai and Shimizu, 1984 . Peak concentrations of
Ž . Ž
estradiol 30–35 pgrml were detected on the day of estrus or one day before Batra and
.
Pandey, 1982 , followed by a decline to 5–10 pgrml within two days. This pattern is
indicative of enhanced estradiol production by the preovulatory follicle during proestrus.
Ž .
Circulating concentrations of LH reached a peak 20–35 ngrml at the onset of estrus
Ž .
followed by a sharp decrease within a day; LH remained low 1–3 ngrml during the
Ž .
luteal phase Batra and Pandey, 1982; Kanai and Shimizu, 1984 . The duration of the
Ž
LH surge has been estimated to be 7–12 h Batra and Pandey, 1982; Kanai and Shimizu,
.
1986 . Peak LH concentrations were estimated to occur about 14.8 h after the peak in
Ž . Ž .
estradiol concentration Batra and Pandey, 1982 . Higher FSH levels 57–65 ngrml
have been observed during the beginning of estrous cycle than during the luteal phase
Ž10–17 ngrml; Razdan et al., 1982 but such a difference was not observed by others.
ŽJanakiraman et al., 1980 . For changes in hormone profiles during different seasons, the.
reader is referred to the section under endocrine alterations during summer.
6. Seasonality
6.1. Seasonal behaÕior
There is a complex dependency of bovine reproduction on soil, plant and climatic
Ž .
Ž
display of estrus, conception rate, and calving rate Ahmad et al., 1980; Madan, 1988; Singh and Nanda, 1993; Singh and Singh, 1985; Singh et al., 1989; Parsha et al., 1986;
.
Shah, 1988; Tailor et al., 1990 . Buffaloes and Zebu cows located at the same farms in
Ž .
Pakistan i.e., managed under similar fodder and climatic conditions showed a different pattern of breeding. The breeding frequency in buffaloes was highest during the winter,
Ž .
decreased in autumn and spring, and was lowest in the summer Shah, 1988 . The Zebu cattle in this study exhibited the opposite seasonal variation; breeding frequency was highest during the summer. Results of other studies done in India are consistent with the Pakistan study; 64% to 75% of buffaloes exhibited estrus during September to January
ŽSingh and Nanda, 1993; Singh and Singh, 1984; Tailor et al., 1990 ..
The interval to first postpartum estrus is also significantly affected by the season of
Ž
calving Basu, 1962; Reddy et al., 1986; Madan, 1988; Singh, 1993; Singh and Nanda,
.
1993 . Buffaloes calving in late winter and early summer have lower reproductive
Ž
efficiency compared to those calving during other periods Siddappa and Patil, 1979;
.
Madan and Raina, 1984; Singh and Nanda, 1993 . The resumption of ovarian activity after calving was significantly delayed in buffaloes that calved from February to May
Ž116–148 days compared to the rest of the year 38–64 days; Singh and Nanda, 1993 .. Ž .
Ž .
Futhermore, conception rates were lower between February and August Madan, 1988 , and number of services per conception was higher in summer calvers than those calving in other seasons.
Ž
In rural Punjab lat 298 to 328N, long 758to 768E; temperature extremes: 08–468C;
. Ž .
day length: 10–14 h most buffaloes 58% are pregnant during the heat of the summer.
Ž .
However, among the remaining nonpregnant buffaloes, the majority 77% become
Ž .
anestrus during the hot summer months Singh et al., 1989 . Seasonal suppression
Žsummer versus winter of reproductive function has been documented by a shorter.
Ž .
duration of estrus 8–10 versus 18 h; Janakiraman, 1978 , apparent prolongation of the
Ž
interval from estrus to ovulation 15.8"0.4 versus 14.9"0.4 h in Nagpuri buffaloes;
. Ž
Raut and Kadu, 1988 , and fewer ovulatory cycles 71% versus 92%; Janakiraman,
. Ž .
1978 during the summer months. Unobserved silent estrus and abbreviated duration of
Ž .
estrus are common in swamp buffalo during the summer Kanai and Shimizu, 1983 . In
Ž . Ž
one study Singh et al., 1985 , the incidence of true anestrus defined as the absence of
.
large follicles and CL in the ovaries was 78% in July and 14% in November. Poor libido and semen quality of bulls may also contribute to lower fertility during the summer.
6.2. Endocrine alterations during summer
There is no consensus among studies on the effects of season on the function of the corpus luteum. Some authors suggest that luteal function is adversely affected during the
summer season; maximum circulating concentrations of progesterone were 2.0"1.2
Ž
ngrml during the summer versus 3.1"0.2 ngrml during the winter Rao and Pandey,
.
1982 . Others report that higher concentrations of progesterone were recorded during
Ž
summer than during fall and winter Shafie et al., 1982; Takkar et al., 1983; Singh and
.
Chaudhary, 1992 . Still others detected similar progesterone concentrations during the
Ž .
summer and winter months 1.3"0.4 and 1.3"0.2 ngrml, respectively , but found
Ž .
Ž
Lower circulating concentrations of FSH measured during estrus and during the
. Ž
luteal phase were detected during summer than winter months Janakiraman et al.,
.
1980; Razdan et al., 1982 . Lower LH values during summer than winter have also been
Ž . Ž .
reported by some Rao and Pandey, 1983 , but not by others Sheth et al., 1978 . No optimum LH peak was detected in anestrus versus cycling buffaloes during summer
ŽRazdan and Kaker, 1980; Razdan et al., 1984 . The amplitude and frequency of LH.
secretion during the follicular phase were lower during the summer than during the
Ž .
winter Aboul-Ela and Barkawi, 1988 . Furthermore, a lower LH pulse frequency during
Ž . Ž .
the luteal phase was observed in the summer 2.1r8 h than winter 3.2r8 h .
6.3. Factors affecting seasonal behaÕior
It is not clear to what extent the seasonal breeding pattern is a genetic characteristic of buffalo or a result of environmental factors. However, evidence suggests a strong
Ž
influence of biometeorological factors on the endocrine system of buffaloes i.e., day
.
length, ambient temperature, relative humidity and rain fall; Shah, 1988 . The seasonal pattern may also be attributed to be a consequence of, or adjustment to, meager availability of green fodder during the summer months. However, that this is not the sole factor affecting seasonality is borne out by the results of the Pakistan study in which buffalo displayed a different breeding pattern than cattle kept under similar
environmen-Ž .
tal conditions Shah, 1988 . Greater breeding activity was detected during autumn in buffaloes than in cattle. On the hot, humid plains of Papua New Guinea, most swamp buffaloes continued to come into heat despite losing weight due to poor nutrition, while
Ž .
cows kept under the same conditions became anestrus Report, 1981 .
Further, reduced sexual activity in the buffalo coincides with both an increase in
Ž .
ambient temperature Dessoukey and Juma, 1973; Singh et al., 1989 and increasing day
Ž .
length Razdan and Kaker, 1980 , but studies done to date have not been designed to distinguish between the effects of photoperiod and other environmental factors. The incidence of true anestrus was significantly correlated with mean maximum and
Ž .
minimum air temperature rs0.8 and 0.9, respectively and with mean relative
Ž .
humidity rs y0.7; Singh et al., 1985 . The proportion of buffaloes exhibiting estrus
during the period of short day length was significantly greater than during the period of
Ž .
long day length 74% versus 26%, respectively; Tailor et al., 1990 .
Ž
In an elaborate study examining the interval from parturition to first estrus Singh,
.
1993; Singh and Nanda, 1993 , data collected during two successive years were compared to distinguish between the effects of photoperiod and other environmental
Ž
factors i.e., successive years had the same photoperiod changes, but different rainfall
.
and ambient temperature patterns . Only 23% of all detected estrus were recorded in the months with increasing temperature, suggesting some suppressive effects of higher
Ž .
temperatures Fig. 1 . However, the highest temperature was recorded in June whereas the lowest incidence of estrus was in July. Moreover, 15% of estrus observations occurred in September versus only 5% in March despite a similar temperature during
Ž .
these 2 months. Relative humidity was maximum in January 74% and minimum in
Ž .
Fig. 1. Percent distribution of display of first estrus after calving by buffaloes during a 1-year interval in
Ž
relation to day length, ambient temperature and relative humidity in Punjab, India data adapted from Singh,
.
1993; Singh and Nanda, 1993 .
Ž .
through June, the relative humidity was higher and the temperature was lower P-0.05
in 1986 than in 1985 due to early rainfall; however, no difference in the incidence of
Ž
estrus was detected between years. Day length was also negatively correlated rs y0.7,
.
P-0.01 with the interval from parturition to first estrus. These patterns indicate that decreasing day length may be a stronger determinant of the onset of postpartum ovarian activity, whereas ambient temperature and relative humidity may have relatively lesser influence.
7. Estrus synchronization
Covert or silent estrus constitutes the single largest factor responsible for poor reproductive efficiency in buffalo. Aside from seasonal factors affecting the display of estrus, the most important contributing factor is an inability to detect estrus. The traditional farmer possesses only one to four buffaloes and usually no bull; hence, there is little opportunity for behavioral interaction among estrous animals. Artificial control of the estrous cycle has provided an efficient means of increasing the reproductive capacity of buffalo by obviating the need for frequent visual inspections.
Progesterone-Ž .
or norgestomet-containing devices injections, PRID, pessaries, CIDR, ear implants
Ž .
along with PMSG, estradiol andror prostaglandin PGF2a have been used successfully
Ž
to improve synchrony of estrus and conception in buffalo Rao and Rao, 1979, 1983;
.
Rao et al., 1985; Singh et al., 1983; Saini et al., 1986; Chohan et al., 1995 . Results of
Ž
obtained in cattle Kamonpatana et al., 1979; Pathiraja et al., 1979, Pant and Singh, 1980; Kamonpatana et al., 1987; Rao and Venkatramaiah, 1989; Dhaliwal and Sharma,
.
1990; Dhaliwal et al., 1987; Sahasrabudhe and Pandit, 1997 . The endocrine changes following PGF2ayinduced luteolysis appear to be similar to those occurring at natural
Ž .
estrus Kamonpatana et al., 1979 . In addition, use of one fifth the conventional dose of PGF2a by intravaginal submucosal injection was equally as effective in inducing estrus
Ž
as conventional treatment Rao and Rao, 1988; Rao and Venkatramaiah, 1989;
Subrama-. Ž .
niam et al., 1989 . However, results of others Dhaliwal et al., 1987 suggested that the intravaginal route was not as effective for inducing synchrony as conventional treatment for fixed-time insemination. Better synchrony and conception rates have been
docu-Ž .
mented after synchronization during the breeding season winter than the nonbreeding
Ž . Ž .
season summer; Rao and Rao, 1983 , but a remarkably high percentage 88% of
subestrous buffaloes expressed standing estrus after PGF2a treatment during the hot
Ž .
summer months Sahasrabudhe and Pandit, 1997 .
8. Multiple ovulations in response to exogenous gonadotropins
The ovarian response of buffaloes to superstimulatory treatment has been less than
one third of that reported in cattle. By using Folltropinw, SuperOVw, FSH-Pw or
Ž .
PMSG, only 50% to 55% of bufflaloes respond i.e., )2 ovulations , and of those that
respond, only two to four ovulations are induced, producing only one to two transferable
Ž
embryos Parnpai et al., 1985; Karaivanov, 1986; Vlakhov et al., 1986; Alexiev et al., 1988; Sharifuddin and Jainudeen, 1988; Singh et al., 1988; Singla and Madan, 1990;
.
Misra et al., 1991; Kasiraj et al., 1992; Agarwal et al., 1996 . Although experiments on multiple ovulation in buffalo were initiated over three decades ago, systematic examina-tion of the ovarian response to gonadotropin treatment relative to intrinsic follicular development has not been done. The world’s first buffalo calf through embryo transfer
Ž .
was born in the USA in 1983 Drost et al., 1983 .
Ž
Various schedules of gonadotropin treatment, such as PMSG Parnpai et al., 1985; Vlakhov et al., 1986; Karaivanov, 1986; Alexiev et al., 1988; Nanda and Bhat, 1988;
. Ž
Misra, 1993 , tapering doses of FSH Singh et al., 1988; Singla and Madan, 1990; Misra
. Ž .
et al., 1991 , and single injection of FSH Kasiraj et al., 1992 have been adopted from superovulatory protocols in cattle. Higher ovulation rates have been reported when
Ž .
gonadotropin treatment was initiated during the mid-luteal phase Day 12 than the early
ŽDay 3–6 or late luteal Day 13–15 phase Mehmood et al., 1988; Karaivanov et al.,. Ž . Ž .
1990 . Higher ovulations were achieved when treatments were initiated in the absence of
Ž .
a dominant follicle than the presence Taneja et al., 1995 .
9. Conclusion
There is a strong need to identify the factors responsible so as to devise effective breeding strategies. In addition, current knowledge of basic and seasonal patterns of follicle development in the buffalo is insufficient. Efforts may be directed at
understand-Ž . Ž
ing the process recruitment, development, atresia and temporal pattern follicle selec-tion, dominance, subordinate follicle suppression, follicle numbers, and, preovulatory
.
changes of follicular dynamics using techniques which permit serial assessment of changes occurring over time. Emphasis may be directed towards investigating follicular ‘‘waves’’ as a functional unit, rather than the estrous cycle, in the context of whole animal endocrinology. The data obtained from such basic studies may then be used to develop and test models for enhancing reproductive efficiency. It would be particularly interesting to determine responses to treatment in relation to the intrinsic pattern of follicle development. The existence of a wave-pattern of follicular dynamics in buffaloes and temporal relationships among follicles may be expected to impact directly on the design of, and reponse to, synchronization and superstimulation protocols. In addition there is strong need for a concerted and organized effort to produce purified native and recombinant gonadotropins for developing buffalo-specific immunoassays and for thera-peuticrsuperovulatory treatments.
References
Aboul-Ela, M.B., Barkawi, A.H., 1988. Pulsatile secretion of LH in cycling buffalo heifers as affected by season and stage of oestrous cycle. In: Proc. 11th Int. Congr. on Anim. Reprod. and Artificial Insemina-tion, Dublin vol. 2, p. 3.
Agarwal, S.K., Purbey, L.N., 1983. Oestrus behaviour and its relation to conception in rural buffaloes. Indian Vet. J. 60, 631–636.
Agarwal, S.K., Tomar, O.S., 1998. Reproductive Technologies in Buffalo. Indian Vet. Res. Inst., Izatnagar, India.
Agarwal, S.K., Shankar, U., Yadav, M.C., 1996. The effect of priming with follitropin in early cycle on superovulatory response and quality of embryos in buffaloes. Buffalo J. 12, 207–211.
Ahmed, A., Agarwal, S.P., Agarwal, V.K., Rahman, S.A., Laumas, K.R., 1977. Steroid hormones: Part II. Serum progesterone concentration in buffaloes. Indian J. Exp. Biol. 15, 591–593.
Ahmad, N., Chaudhry, R.A., Khan, B.B., 1980. Effect of month and season of calving on the length of subsequent calving interval in Nili-Ravi buffaloes. Anim. Reprod. Sci. 3, 301–306.
Alexiev, A., Vlakhov, K., Karaivanov, Ch., Kacheva, D., Palikhronov, O., Petrov, M., Nikolov, N., Drogoev, A., Radev, P.C., 1988. Embryo transfer in buffaloes in Bulgaria. In: Proc. 2nd World Buffalo Congr. vol. 2, pp. 591–595.
Arora, R.C., Pandey, R.S., 1982. Changes in peripheral plasma concentrations of progesterone, estradiol-17
Ž .
beta, and luteinizing hormone during pregnancy and around parturition in the buffalo Bubalus bubalis . Gen. Comp. Endocrinol. 48, 403–410.
Bachlaus, N.K., Arora, R.C., Prasad, A., Pandey, R.S., 1979. Plasma levels of gonadal hormones in cycling buffalo heifers. Indian J. Exp. Biol. 17, 823–825.
Basu, S., 1962. Seasonal variation in fertility in Murrah buffaloes. Indian Vet. J. 39, 433–438.
Batra, S.K., Pandey, R.S., 1982. Luteinizing hormone and oestradiol-17bin blood plasma and milk during the oestrous cycle and early pregnancy in Murrah buffaloes. Anim. Reprod. Sci. 5, 247–257.
Chohan, K.R., Iqbal, J., Choudhary, R.A., Khan, A.H., 1995. Oestrous response and fertility in true anoestrus buffaloes following hormonal treatment during summer. Pakistan Vet. J. 15, 6–8.
Danell, B., Gopakumar, N., Nair, M.C.S., Rajgopalan, K., 1984. Heat detection symptoms in Surti buffalo breeds. Indian J. Anim. Reprod. 5, 1–7.
Dessoukey, F., Juma, K.M., 1973. Infertility problems among cows and buffaloes in Iraq. Indian J. Anim. Sci. 43, 187.
Dhaliwal, G.S., Sharma, R.D., 1990. Serum progesterone profiles in buffaloes following two routes of PGF2-alpha administration. Indian J. Anim. Sci. 60, 967–968.
Dhaliwal, G.S., Sharma, R.D., Biswas, R.K., 1987. Comparative fertility in buffaloes with observed and timed insemination using two routes of PGF2a administration. Vet. Rec. 121, 475–476.
Ž
Drost, M., Wright, J.M. Jr., Cripe, W.S., Richter, A.R., 1983. Embryo transfer in water buffalo Bubalus .
bubalis . Theriogenology 20, 579–584.
El-Wishy, A.B., Abdu, M.S.S., Hemoudas, N., El Saway, S.A., 1971. Reproduction in buffaloes in Egypt: morphological features of the ovaries of cattle and buffaloes in relation to their function. Z. Tierz. Zuechtungsbiol. 88, 47–63.
Erickson, B.H., 1966. Development and senescence of the postnatal bovine ovary. J. Anim. Sci. 25, 800–805. Fadle, W.S.A., Fahmy, M.F.A., El Shafey, S.M., 1974. Histological studies on the ovaries of Egyptian buffaloes with special reference to the corpus luteum. Zentralbl. Veterinaermed., Reihe A 21, 581–591. Janakiraman, K., 1978. Control and optimizing reproductive cycle in buffaloes. In: Proc. FAOrSIDA Seminar
on Buffalo Reprod. and Artificial Insemination, India.
Janakiraman, K., Desai, M.C., Amin, D.R., Sheth, A.R., Moodbidri, S.B., Wadadekar, K.B., 1980. Serum gonadotropin levels in buffaloes in relation to phases of oestrous cycle and breeding periods. Indian J. Anim.Sci. 50, 601–606.
Kamizi, S.E., 1983. Observations on behavioural changes during oestrus in Nili-Ravi buffalo heifers. Pakistan Vet. J. 3, 88–90.
Kamonpatana, M., Kunawongkrit, A., Bodhipaksha, P., Luvira, Y., 1979. Effect of PGF2a on serum
Ž .
progesterone levels in the Swamp buffalo Bubalus bubalis . J. Reprod. Fertil. 56, 445–449.
Kamonpatana, M., Pansin, C., Srisakwattana, K., Paranpai, R.V., Sophon, S., Sravasi, S., Tasripu, K., Doenghana, N., 1987. Buffalo J. Suppl. 1, 1–22.
Kanai, Y., Shimizu, H., 1983. Characteristics of the estrous cycle of the Swamp buffalo under temperate conditions. Theriogenology 19, 593–602.
Kanai, Y., Shimizu, H., 1984. Plasma concentration of luteinizing hormone, progesterone and oestradiol
Ž .
during the oestrous cycle in swamp buffaloes Bubalus bubalis . J. Reprod. Fertil. 70, 507–510. Kanai, Y., Shimizu, H., 1986. Changes in plasma concentration of luteinizing hormone, progesterone and
Ž .
oestradiol-17beta; during the periovulatory period in cyclic swamp buffaloes Bubalus bubalis . Anim.
Reprod. Sci. 11, 17–24.
Karaivanov, C., Kacheva, D., Petrov, M., Vlahov, K., Sapundjiev, E., 1990. Superovulatory response of river
Ž .
buffalo Bubalus bubalis . Theriogenology 33, 453–464.
Karaivanov, Ch., 1986. Comparative studies on the superovulatory effect of PMSG and FSH in water buffalo
ŽBubalus bubalis . Theriogenology 26, 51–59..
Kasiraj, R., Rao, M.M., Rangareddy, N.S., Misra, A.K., 1992. Superovulatory response in buffaloes following single subcutaneous or multiple intramuscular FSH administration. Theriogenology 37, 234.
Kumar, R., Rattan, P.J.S., 1992. Seasonal variation in gonadal and hypophyseal hormones in pre-pubertal buffalo heifers. Indian J. Anim. Reprod. 13, 63–65.
Kumar, A., Solanki, V.S., Jindal, S.K., Tripathi, V.N., Jain, G.C., 1997. Oocyte retrieval and histological studies of follicular population in buffalo ovaries. Anim. Reprod. Sci. 47, 189–195.
Luktuke, S.N., Ahuja, L.D., 1961. Studies on ovulation in buffaloes. J. Reprod. Fertil. 2, 200–201. Madan, M.L., 1988. Status of reproduction in female buffalo. In: Buffalo Production and Health: a
compendium of latest research information based on Indian studies. ICAR Publication, New Delhi, India, pp. 89–100.
Madan, M.L., Raina, V.S., 1984. Fertility and performance of buffaloes under tropical conditions. In: 10th Int. Congr. on Anim. Reprod. and Artificial Insemination, Illinois vol. 2, pp. 142.1–142.4.
Mehmood, A., Anwar, M., Javad, M.H., 1988. Superovulation with PMSG beginning on three different days of the cycle in Nili-Ravi buffaloes. Buffalo J. 5, 79–84.
Misra, A.K., 1993. Superovulation and embryo transfer in buffaloes: progress, problems and future prospects in India. Buffalo J. 9, 1–13.
Misra, A.K., Joshi, B.V., Kasiraj, R., Sivaiah, S., Rangareddi, N.S., 1991. Improved superovulatory regimen
Ž .
for buffalo Bubalus bubalis . Theriogenology 35, 245.
Nanda, S.K., Bhat, P.N., 1988. Superovulation effects of PMSG and FSH in Indian Buffaloes. In: Proc. 2nd World Buffalo Congr. vol. 1, p. 58.
Ocampo, M.B., De. Asis, A.T., Ocampo, L.C., Kanagawa, H., 1994. Histological observation of follicular atresia in Swamp buffalo. Buffalo Bull. 13, 51–55.
Pant, H.C., Singh, G.D., 1980. Control of the estrus cycle in buffaloes with a synthetic analogue of
Ž .
prostaglandin F2 alpha ICI 80996 . Indian Vet. J. 57, 870–871.
Parnpai, R., Timsard, V., Kamonpatana, M., Pansin, C., Sophon, S., Jetana, T., Limsakul, A., Austin, C.R., 1985. Recovery of Swamp buffalo embryo using non-surgical technique. Buffalo J. 1, 77–82.
Parsha, T.N., Chaudhary, M.A., Jabbar, M.A., 1986. Effect of month and season on breeding behaviour of Nili-Ravi buffaloes in rural conditions. Buffalo J. 2, 135–139.
Pathiraja, N., Abeyratne, A.S., Perera, B.M.A.O., Buvanendran, V., 1979. Fertility in buffaloes after oestrus synchronisation with cloprostenol and fixed time insemination. Vet. Rec. 104, 279–281.
Predojevic, R.M., Miljkovic, V., Perkovic, S., Subotin, L., 1988. The role of climatic factors in bovine reproduction. In: 11th Int. Congr. on Anim. Reprod. and Artificial Insemination, Dublin vol. 3, p. 415. Rao, A.R., Rao, C.C., 1983. Synchronisation of oestrus and fertility in buffaloes with a progesterone releasing
intravaginal device. Vet. Rec. 113, 623.
Rao, A.R., Rao, S.V., 1979. Synchronisation of oestrus in buffaloes with norgestomet. Vet. Rec. 105, 256. Rao, A.V.N., Venkatramaiah, P., 1989. Luteolytic effect of a low dose of cloprostenol monitored by changes
in vaginal resistance in suboestrous buffaloes. Anim. Reprod. Sci. 21, 149–152.
Rao, A.V.N., Sreemannarayana, O., Rao, K.P., 1985. Oestrous response and fertility in post-partum anoestrous buffaloes treated with a progestagen, pregnant mares’ serum gonadotrophin and prostaglandin during the low breeding season. Anim. Reprod. Sci. 8, 129–135.
Rao, K.H., Rao, A.V.N., 1988. Luteolytic effect of a small dose of Cloprostenol administered via intravulval route in riverine buffaloes. In: Proc. 2nd World Buffalo Congr. vol. 3, pp. 159–161.
Rao, L.N., Pandey, R.S., 1982. Seasonal changes in plasma progesterone concentrations in buffalo cows
ŽBubalus bubalis . J. Reprod. Fertil. 66, 57–61..
Rao, L.N., Pandey, R.S., 1983. Seasonal variations in oestradiol 17band luteinizing hormone in the blood of
Ž .
buffalo cows Bubalus bubalis . J. Endocrinol. 98, 251–255.
Rao, N.M., Kodagali, S.B., 1983. Onset of oestrus signs and optimum time of insemination in Surti buffaloes
ŽIndia . Indian J. Anim. Sci. 53, 553–555..
Ž .
Raut, N.V., Kadu, M.S., 1988. Observations on ovulation and its association with fertility in Berari Nagpuri buffaloes. In: 11th Int. Congr. on Anim. Reprod. and Artificial Insemination vol. 3, p. 542.
Razdan, M.N., Kaker, M.L., 1980. Summer subfertility and endocrine profiles of buffalo. Indian Dairyman 32, 459–463.
Razdan, M.N., Kaker, M.L., Galhotra, M.M., 1982. Serum FSH levels during estrus and a 4-week period
Ž .
following mating in Murrah buffaloes Bubalus bubalis . Theriogenology 17, 175–181.
Razdan, M.M., Kaker, M.L., Galhotra, M.M., 1984. Serum FSH, LH and PRL levels of cycling and
Ž .
non-cycling Murrah buffaloes Bubalus bubalis . In: Proc. 10th Int. Congr. on Anim. Reprod. and
Artificial Insemination, Illinois vol. 2, p. 16.
Reddy, A.O., Tripathi, V.N., Raina, V.S., 1986. Factors affecting postpartum reproductive efficiency in Murrah buffaloes. Indian J. Anim. Sci. 56, 1224–1228.
Report, 1981. The Water Buffalo: New Prospects for an Under Utilized Animal. National Academy Press, Washington, DC.
Roy, D.J., Mullick, D.N., 1964. Endocrine functions of corpus luteum of buffaloes during estrus cycle. Endocrinology 75, 284–287.
Sahasrabudhe, S.A., Pandit, R.K., 1997. PGF2a induced oestrus in suboestrus Murrah buffaloes during summer. Indian J. Anim.Sci. 67, 513–514.
Ž .
non-cyclic buffalo Bubalus bubalis heifers with progesterone releasing intravaginal device and pregnant mare serum gonadotrophin and their gonadotrophin profile. Theriogenology 26, 749–755.
Samad, H.A., Hamid, A., Rehman, N.V., 1988. In: Proc. 11th Int. Congr. On Anim Reprod. and Artificial Insemination, Dublin vol. 2, p. 68.
Samad, H.A, Nasseri, A.A., 1979. A quantitative study of primordial follicles in buffalo heifer ovaries. In: Compendium, 13th FAOrSIDA Int. Course on Anim. Reprod., Uppasala, Sweden.
Shafie, M.M., Mourad, H., Barakawi, A., Aboul-Ela, M.B., Mekawy, Y., 1982. Serum progesterone and oestradiol concentration in the cycling buffaloes. Trop. Anim. Prod. 7, 301–308.
Shah, S.N.H., 1988. Comparative studies of seasonal influence on breeding behaviour and conception rate of dairy buffalo and zebu cattle. In: Proc. 11th Int. Congr. on Anim. Reprod. and Artificial Insemination vol. 3, p. 538.
Ž .
Sharifuddin, W., Jainudeen, M.R., 1988. Embryo collection in the Swamp buffalo Bubalus bubalis . In: 11th Int. Congr. on Anim. Reprod. and Artificial Insemination vol. 3, p. 543.
Sheth, A.R., Wadaker, K.B., Moodbidri, S.B., Janakiraman, J., Parameswaran, M., 1978. Seasonal alteration in the serum prolactin and LH levels in the water buffalo. Curr. Sci. 47, 75–77.
Ž .
Shimizu, H., 1987. Embryo collection in the Swamp buffalo Bubalus bubalis . In: Proc. Int. Seminar on Milk Buffalo Reprod., Islamabad, Pakistan, March.
Siddappa, T.N., Patil, S.H., 1979. Seasonality of breeding and calving of buffaloes. Indian Vet. J. 56, 122–124.
Singh, C.S.P., Singh, B., 1984. Incidence of oestrus in buffalo. Indian J. Anim. Sci. 54, 259–260.
Singh, G., Singh, G.B., 1985. Effect of month of calving on postpartum interval and service period in Murrah buffaloes. In: Proc Ist. World Buffalo Congr., Cairo, Egypt vol. 4, pp. 960–963.
Singh, G., Singh, G.B., Bains, G.S., 1985. Studies on incidence of anoestrus in village buffaloes. Indian J. Anim. Res. 19, 57–60.
Singh, G., Singh, G.B., Dhaliwal, G.S., 1989. Studies on reproductive status of rural buffaloes in summer. Indian J. Anim. Reprod. 10, 151–153.
Singh, G., Singh, G.B., Sharma, R.D., Nanda, A.S., 1983. Experimental treatment of summer anoestrous-buf-faloes with norgestomet and PRID. Theriogenology 19, 323–329.
Singh, G., Singh, G.B., Sharma, S.S., 1984. Studies on follicular patterns in buffalo heifers. Theriogenology 22, 453–462.
Singh, M., Sodi, M.S., Mathroo, J.S., Sharma, R.D., Takkar, O.P., Karaivanov, C.H., Alexiev, A., 1988. Embryo transfer in buffaloes:s. 1. Response of various hormonal regimes on superovulation. In: Proc. 2nd World Buffalo Congr. vol. 1, p. 106.
Ž
Singh, N., Chaudhary, K.C., 1992. Plasma hormonal and electrolyte alterations in cycling buffaloes Bubalus
.
bubalis during hot summer months. Int. J. Biometeorol. 36, 151–154.
Singh, R., 1993. Studies on the onset of postpartem ovarian activity in relation to climatic and nutritional status in buffaloes. MVSc thesis, Punjab Agric., Univ., Ludhiana, India.
Singh, R., Nanda, A.S., 1993. Environmental variables governing seasonality in buffalo breeding. J. Anim.
Ž .
Sci. 71, 119, abstr. .
Ž .
Singla, S.K., Madan, M.L., 1990. Response of superovulation in buffaloes Bubalus bubalis with Super-Ov and FSH-P. Theriogenology 33, 327.
Subramaniam, A., Sundarsingh, J.S.D., Devarajan, K.P., 1989. Estrus synchronization with PGF2 alpha in buffaloes. Indian Vet. J. 66, 538–540.
Tailor, S.P., Jain, L.S., Gupta, H.K., Bhatia, J.S., 1990. Oestrus and conception rates in buffaloes under village conditions. Indian J. Anim. Sci. 60, 1020–1021.
Takkar, O.P., Singh, M., Verman, P.N., 1983. Progesterone levels vis a vis anoestrum in buffaloes concurrent with profile during stages of oestrus cycle. Indian J. Dairy Sci. 36, 125–128.
Taneja, M., Totey, S.M., Ali, A., 1995. Seasonal variation in follicular dynamics of superovulated Indian water buffalo. Theriogenology 43, 451–464.
Ty, L.V., Chupin, D., Driancourt, M.A., 1989. Ovarian follicular populations in buffaloes and cows. Anim. Reprod. Sci. 19, 171–178.
Vlakhov, K., Karaivanov, Kh., Petrov, M., Kacheva, D., 1986. Superovulation and the production of embryos
Ž .
