Effect of weaning on postpartum reproductive performance of Murrah buffaloes

V V Rijasnaz, H O Pandey, B H M Patel, A K S Tomar, S K Mondal and G Singh*

Division of Livestock Production and Management
* Nuclear Research Laboratory
Indian Veterinary Research Institute
Izatnagar, Bareilly, Uttar Pradesh 243 122 India
sk_mondal@yahoo.com

Abstract

The present study was carried out to evaluate the effect of weaning of calves on resumption of ovarian cyclicity and fertility response in postpartum buffaloes. A total of 16 Murrah buffaloes were selected as per their due date of calving and randomly divided into two equal groups i.e. Group S (Suckling) and Group W (Weaned). The animals in the weaning group (n=8) were isolated from their calves by day 3 after calving and animals in suckling (n=8) group were allowed to suckle twice daily. Changes in the progesterone concentration were used to assess the resumption of ovarian cyclicity.

The postpartum interval to resumption of ovarian cyclicity were similar for S and W groups (26.0±0.0 vs. 27.8±1.81 days; P>0.05). However, the interval from calving to the onset of behavioural oestrus was significantly (P<0.01) shorter in W than S(53.3±7.52 vs. 128.0±9.94 days). Significantly more incidence of silent ovulation was observed in W than S buffaloes (75% vs. 12.5%; P<0.01). More than half of animals in W conceived before 90 days postpartum compared to none in S (62.5% vs. 0.0%, P<0.01). First service conception rate in W was slightly greater than in S (28.6% vs. 25.0%). From the present study, it can be concluded that weaning accelerates resumption of ovarian cyclicity and enhances conception rate in Murrah buffaloes. The present findings indicated that weaning could be a rational management strategy for reducing the postpartum anoestrus by earlier resumption of reproductive function in buffaloes. 

Key words: Anoestrus, fertility, ovarian cyclicity, serum progesterone

Introduction

In tropical countries like India, buffaloes are an important livestock resource to millions of dairy farmers. Buffaloes constitute only 35% of the total bovine population in India, but account for more than half of the total milk production in the country (59.2 million tonnes; GOI 2010). However, Indian buffaloes are considered difficult breeders because of their inherent susceptibility to environmental stress which causes anoestrus and repeat breeding, besides delayed age at first calving, longer calving interval and higher incidence of silent ovulation (Usmani et al 1985, Madan 1988) Delayed postpartum oestrus, and therefore conception, affect productivity and cause economic losses to buffalo producers. Various attempts to regulate postpartum reproduction through use of hormones and biological agents have so far failed to be consistently effective and besides, some of these are not easily available, unsustainable or expensive for Indian farmers. For harnessing the reproductive potential of buffaloes, there is a need to develop rational management strategies that will curtail postpartum reproductive problems, without reducing milk yield or calf growth rate. Weaning represents a relatively inexpensive management tool. Cows suckled ad libitum have longer intervals to first oestrus and/or ovulation than cows that have been weaned (Bellows et al 1974). Yavas and Walton (2000) also reported that cyclicity resumes within 2 to 3 weeks postpartum in milked dairy cows, while it does not resume for 35 to 60 d or even longer in suckled beef cows. While there is overwhelming evidence to support the effect of weaning in inducing earlier return to postpartum oestrus in cattle, there exists a paucity of information concerning this application in postpartum buffaloes. Therefore, the present study was undertaken to investigate whether weaning of calves can induce the early resumption of ovarian cyclicity and enhance fertility response in postpartum buffaloes. 

Materials and methods 

Location and climate

The present study was conducted at Cattle and Buffalo Farm, Indian Veterinary Research Institute, Izatnagar, Bareilly, India, during October to June in 2011. This farm is located at an altitude of 169.2 masl (28º 22’N and 79º 24’E) with atmospheric temperature ranging from one extreme (about 5ºC) to other (approx. 48ºC) during the experimental period. 

Experimental animals

A total of 16 multiparous apparently healthy Murrah buffaloes were selected from a herd of 190 buffaloes of advanced stage of pregnancy. They were randomly divided into two equal groups i.e. Group S (Suckling) and Group W (Weaned) at 7 days prior to calving based on body weight (587±25.7 kg and 570±20.2 kg; P>0.05), age (8.6±0.9 years and 7.6±0.8 years; P>0.05) and parity (3.0±0.3 vs. 2.8±0.3; P>0.05). The calves of the animals in the weaning group (n=8) were separated by day 3 postpartum and animals in suckling group (n=8) were allowed to suckle twice daily their own calves. The buffaloes were maintained under loose housing system at the Institute Cattle and Buffalo Farm, where the suckled group of buffaloes was kept just beside the calf shed with a iron pipe fencing. Suckling by calf was allowed twice (Morning and Evening) daily during milking time only. The actual contact time was 5 minutes prior to milking to 15 minutes post-milking. During milking the calf was stanchione in front of the dam. During other parts of the day, the calves were kept separated in a pen with open railings, and in sight of their dams. All buffaloes were between the second and the sixth parity and were free from history of any reproductive disorder. They were maintained in loose houses under similar management conditions and were stall-fed with free access to concentrate mixture and fodder provided in open paddock area twice a day apart from feeding concentrate during milking time. Fresh and clean drinking water was made available throughout day and night. All the animals were hand-milked twice daily until the end of the experiment. 

Heat detection and reproductive parameters

Various reproductive parameters were monitored from calving to day 150 postpartum. The interval to postpartum ovarian cyclicity was recorded. Onset of oestrus in all the animals was checked twice daily (08:30 hours and 17:00 hours) by teaser bull parading and confirmed by examination of genitalia per rectum. Animals in oestrus were artificially inseminated using 0.5 ml frozen–thawed semen of proven fertile buffalo bulls as per the laid down breeding plan of the farm. Pregnancy was preliminarily ascertained in all animals by non-return rate and subsequently confirmed by per-rectal examination at 60 days post-insemination.

Sampling procedure and hormonal assay

Blood samples (5 ml) were aseptically collected by jugular venipuncture at 7 day interval from calving to day 28 postpartum and subsequently at 5 day interval from day 28 postpartum to first behavioural oestrus (or insemination). Further, blood samples were also collected at 5 day interval from oestrus (or insemination) to day 35 post-insemination. After collection, serum samples harvested from blood were stored in 1.5 ml eppendrof tubes at -20°C till hormonal assay. The progesterone levels in the serum samples were estimated using solid phase 125I Radioimmunoassay (RIA) kits (Immunotech®, France). The assay sensitivity was 0.05 ng/ml and had an intra- and inter-assay coefficient of variation of <10%. An increase in baseline progesterone concentration in at least two consecutive samples that exceeded 1 ng/ml was used as the criterion for resumption of ovarian cyclicity (Stumpf et al 1992, Berardinelli and Joshi 2005).

Data analysis

The data on various reproductive parameters were subjected to t-test while the data on proportions or percentages were analysed by chi square test (STATS 1998) following the procedures as described by Snedecor and Cochran (1994). 

Results and discussion

The postpartum intervals to resumption of ovarian cyclicity were 27.8±1.81 and 26.0±0.00 days for W and S groups, respectively (P>0.05). But the mean interval to the onset of behavioural oestrus was significantly (P<0.01) shorter in W (53.3±7.52 vs. 128.0±9.94 days) than S (Table 1). A significantly (P<0.01) higher proportion of animals in W (87.5% vs. 12.5%) resumed cyclicity by day 90 postpartum as compared to animals in S. 

Apparently higher incidence of silent ovulation was there in W buffaloes (75%) compared to S animals (12.5%). When the interval from calving to conception (Table 1) was considered, animals in W conceived earlier as compared to S (75.7±10.16 vs. 143.5±5.50 days; P<0.01). Significantly (P<0.01) higher conception rate (62.5%) was recorded in W buffaloes than S buffaloes (0%) within day 90 postpartum. Mean serum progesterone concentration above 1 ng/ ml (Table 2) was observed as early as on day 21 postpartum in W buffaloes (1.49±0.39 vs. 0.80±0.10; P<0.05) indicating early resumption of cyclicity in these animals. 

The significant effect of weaning of calves on the dam’s expression of behavioural oestrus might be due to the removal of suckling stimulus and subsequent series of hormonal changes. Early weaning was shown to be effective in removing the suppressive effects of suckling from the hypothalamo-hypophyseal-gonadal axis (Bell et al 1998). Our findings were consistent with earlier reports of Wells et al (1985) who reported that weaning calves during the first week after calving dramatically reduces the time from calving to the onset of ovarian activity. This is further supported by the findings of Perera (2011) who reported that dairy buffaloes managed with no suckling, resume oestrus cyclicity by 30–60 days after calving. This early resumption of ovarian cyclicity in W indicated a rapid response of these animals to weaning. However, in contrast to these results, weaning calves beyond the first week after calving resulted in varied responses (Maree et al 1974, Salcedo et al 1977, Pimentel et al 1979, Alberio et al 1984, Lishman and Harwin 1985, Thu and Trach 2012). Weaning after day 45 postpartum did not affect the duration of postpartum anoestrus (Yavas and Walton 2000). Weaning by day 60 or day 90 postpartum did not improve postpartum fertility in buffaloes (Qureshi and Ahmad 2008).

Higher proportion of animals in W resumed cyclicity by day 90 postpartum as compared to animals in S. This is in accordance with the earlier findings (Bell et al 1998). Interestingly, in our study weaning stimulated a majority of animals to ovulate before day 40 postpartum. This was important as it allowed them to experience one or two oestrous cycles for successful breeding before 70 – 90 days postpartum, by which buffaloes must be pregnant to maintain a calving interval of 13–14 months (El-Wishy 2007). Apparently higher incidence of silent ovulation was there in W buffaloes (75%) compared to S animals (12.5%). The lack of appropriate male stimuli may be considered as a contributory factor for weak expression of oestrus and higher incidence of silent oestrus in weaned buffaloes. Presence of male has been shown to increase the expression of oestrus in cows (Landaeta Hernandez et al 2006), buffaloes (Zicarelli et al 1997), sheep (Mondal et al 2011), goat (Islam 2010, Mondal et al 2009) and sows (Langendijk et al 2000). Various workers have reported significantly reduced proportion of silent oestrus in bull-exposed cattle (22% vs. 89%; Alberio et al 1987) as well as buffaloes (57.14% vs. 85.71%; Barman 2008).

Animals in W conceived earlier as compared to S and significantly higher conception rate was recorded in W buffaloes than S buffaloes within day 90 postpartum. This indicated that weaning significantly reduced calving-to-conception interval, i.e., service period. Early weaning increased pregnancy rates in some herds of Bos indicus cows (Montiel and Ahuja 2005) but responses varied widely. The findings that suckling ad libitum in buffaloes resulted in lower conception rate (Abeygunawardena et al 1995) are in agreement with our results. In contrary, early weaning had not been shown to affect the postpartum interval to pregnancy or pregnancy rate (Bell et al 1998). Considering the fertility response of weaning induced oestrous cycles, our results further reaffirmed the fact that weaning could enhance the conception rates and reduce calving-to-conception interval in postpartum buffaloes. These findings on increased conception rate as well as higher proportion of animals becoming cyclic within 28 days of weaning indicated weaning-mediated effect on postpartum reproduction in buffaloes.

Mean serum progesterone concentration above 1 ng/ ml was observed as early as on day 21 postpartum in W buffaloes indicating early resumption of cyclicity in these animals. Further, enhanced conception rate as well as higher proportion of cyclic animals in W was indicated by higher progesterone levels (2.50 ng/ ml) during later postpartum period (before day 90).  Weaning may be influencing time of ovulation, fertilization rates, corpus luteum development, progesterone secretion and embryonic survival. Higher serum progesterone concentration during the oestrous cycle (Figure 1) preceding insemination was closely related to the occurrence of conception in postpartum dairy cows (Folman et al 1973). Higher levels of progesterone were observed during the critical period of conception in W buffaloes (Figure 2). Secretion of endogenous LH also might have improved potential development of the corpus luteum and thereby increased progesterone secretion (Kawate et al 2000). Maurer and Echternkamp (1982) found higher embryo survival in cows with higher pre-ovulatory surges of LH and earlier postovulatory rises of luteal progesterone.  Interestingly, suckling reduces the hypothalamic release of GnRH, which results in insufficient pulsatile LH release (Williams 1990). Therefore, it might be a possibility that added increment of LH secretion due to weaning might have some role in the events associated with conception in W buffaloes. Further work needs to be done to elucidate the weaning effect on hormone secretion and its mechanism for improving conception in postpartum buffaloes.

The findings of the present study such as, rapid occurrence of estrus in higher proportion of animals and enhanced conception rate further corroborated the fact that weaning did have influence on postpartum reproductive performance in buffaloes. The weaning-effect observed in the present study may have occurred by the hypothalamo-pituitary-ovarian (HPO) axis to initiate resumption of ovarian activity. The role of vision and olfaction in suckling-mediated inhibition of LH secretion in cattle has been investigated (Griffith and Williams 1994). Again, the maternal-offspring bond is essential for the suckling-induced anovulation and cows can use both olfactory and visual cues to identify own and unrelated offspring (Williams and Griffith 1995). The importance of cow-calf bonding and its relationship to postpartum anovulation was reinforced by Lamb et al (1997). Therefore, further investigation on weaning is necessary to unveil mechanisms associated with weaning as well as to characterize the situations which provoke the maximum reproductive response in postpartum animals.   

Conclusions

• It is obvious from our findings that weaning accelerates postpartum resumption of ovarian cyclic activity and enhances conception rate. Weaning can be an effective strategy to increase the number of pregnant animals during the earlier days of mating period after calving. Incorporation of weaning may help optimize overall reproductive performance in postpartum buffaloes.

Acknowledgements

The authors are thankful to the Director, Indian Veterinary Research Institute, Izatnagar and Head, Livestock Production and Management for providing necessary facilities and logistic support to conduct the study. Financial support provided by Indian Council of Agricultural Research is duly acknowledged. 

References

Abeygunawardena H, Kuruwita V Y and Perera B M A O 1995 SAREC/NARESA Regional Symposium on the Role of the Buffalo in Rural Development in Asia, Plant Genetic Resource Center, Sri Lanka.

Alberio R, Butler H, Palma G, Schiersmann G and Mihura H 1984 Efecto de un destete temporario sobre la reactivación posparto de vacas de cr´ıa prim´ıparas. Revista  Argentina de Produccion Animal 4: 933.

Alberio R H, Schiersmann G, Carou N and Mestre J 1987 Effect of a teaser bull on ovarian and behavioral activity of suckling beef cows. Animal Reproduction Science 14: 263.

Barman P 2008 Identification of urinary compounds, response of estrual and diestrual urine on male libido and effect of bull exposure on ovarian cyclicity in postpartum buffalo. Ph. D. Thesis submitted to Indian Veterinary Research Institute, Izatnagar, U.P., India.

Bell D J, Spitzer J C and Bums G L 1998 Comparative effects of early weaning or once-daily suckling on occurrence of postpartum estrus in primiparous beef cows. Theriogenology 50: 707.

Bellows R A, Short R E, Urick J J and Pahnish O F 1974 Effects of early weaning on postpartum reproduction of the dam and growth of calves born as multiples or singles. Journal of Animal Science 39: 589.

Berardinelli J G and Joshi P S 2005 Introduction of bulls at different days postpartum on resumption of ovarian cycling activity in primiparous beef cows. Journal of Animal Science 83: 2106.

El-Wishy A B 2007 The postpartum buffalo. II. A cyclicity and anestrus. Animal Reproduction Science 97: 216.

Folman Y, Rosenberg M, Herz Z and Davidson M 1973 The relationship between plasma progesterone concentration and conception in postpartum dairy cows maintained on two levels of nutrition. Journal of Reproduction and Fertility 34: 267.

Government of India (GOI) 2010 Basic Animal Husbandry Statistics. Ministry of Agriculture. Department of Animal Husbandry, Dairying and Fisheries. New Delhi.

Griffith M K and Williams G L 1994 Role of visual and olfactory cues during suckling in control of maternal behavior, lactation and suckling-mediated inhibition of LH secretion in beef cows. Journal of Animal Science 72 (Suppl 1): 366.

Islam M M 2010 Studies on buck effect for improving reproductive efficiency in indigenous goats. M.V. Sc. Thesis submitted to Indian Veterinary Research Institute, Izatnagar, U.P., India.

Kawate N, Morita N, Tsuji M, Tamada H, Inaba T and Sawada T 2000 Roles of pulsatile release of LH in the development and maintenance of corpus luteum function in the goat. Theriogenology 54: 1133.

Lamb G C, Lynch J M, Greiger D M, Minton J E and Stevenson J S 1997 Ad libitum suckling by unrelated calf in the presence or absence of a cow’s own calf prolongs postpartum anovulation. Journal of Animal Science 75: 2762.

Landaeta-Hernandez A J, Melendez P, Bartolome J, Rae D O and Archbald L F 2006 Effect of biostimulation on the expression of estrus in postpartum Angus cows. Theriogenology 66: 710.

Langendijk P, Soede N M, Bouwman E G and  Kemp B 2000 Responsiveness to boar stimuli and change in vulvar reddening in relation to ovulation in weaned sows. Journal of Animal Science 78: 3019.

Lishman A W and Harwin G O 1985 Failure to induce ovulation by short-term calf removal in lactating beef cows on dry-lot. South African Journal of Animal Science 15: 21.

Madan M L 1988 Status of reproduction in fermale buffalo. In: Buffalo production and health. ICAR Publication, New Delhi, India 89.

Maree C, Jurriaanse A and Venter H A W 1974 The occurrence of post partum anoestrus in Bonsmara cows on supplemented sourveld grazing. South African Journal of Animal Science 4: 181.

Maurer R R and Echternkamp S E 1982 Hormonal asynchrony and embryonic development. Theriogenology 17: 11.

Mondal S K, Joshi H C, Majumdar A C, Majumdar S, Varshney V P, Dutt Triveni and Pandey H N 2009 Reproductive responses of anoestrous indigenous does to male introduction during postpartum. Indian Journal of Animal Science 79: 554.

Mondal S K, Joshi H C, Majumdar A C, Deb S M, Pandey H N, Varshney V P and Dutt Triveni 2011 The male effect in muzaffarnagari sheep. 1. Ovarian and behavioral responses to male introduction. Journal of Applied Animal Research 39: 275.

Montiel F and Ahuja C 2005 Body condition and suckling as factors influencing the duration of postpartum anestrus in cattle: a review. Animal Reproduction Science 85: 1.

Perera B M A O 2011 Reproductive cycles of buffalo. Animal Reproduction Science 124: 194.

Pimentel C A, Deschamps J C, Oliveira J A F, Cardelino R and Pimentel M A 1979 Effects of early weaning on reproductive efficiency in beef cows. Theriogenology 11: 421.

Qureshi M S and Ahmad N 2008 Interaction of calf suckling, use of oxytocin and milk yield with reproductive performance of dairy buffaloes. Animal Reproduction Science 106: 380.

Salcedo E, González-Padilla E, Rodr´ıguez O L and Ramos F 1977 Efecto del destete precoz en el comportamiento reproductivo de vacas empadradas en agostadero. Cited in Animal Breeding Abstracts.

Snedecor G W and Cochran W G 1994 Statistical methods. 8^th ed. Oxford University Press, London.

STATS 1998 STATS^TM User’s Guide: Release (Version 1.1), Decision analysis, Inc., USA.

Stumpf T T, Wolfe M W, Day M L, Kittok R J and Kinder J E 1992 Weight changes prepartum and presence of bulls postpartum interact to affect duration of postpartum anestrus in cows. Journal of Animal Science 70: 3133.

Thu C T T and Trach N X 2012 Effects of early weaning on postpartum resumption of reproduction in mother buffaloes and growth of their calves.  Livestock Research for Rural Development, Volume 24, Article #19 Retrieved March 3, 2012, from http://www.lrrd.org/lrrd24/1/thu24019.htm

Usmani R H, Ullah N and Shah S K 1985 A note on the effect of suckling stimulus on uterine involution, postpartum ovarian activity and fertility in Nili Ravi buffaloes. Animal Production 41: 119.

Wells P L, Holness D H, Reymark P J, McCabe C T and Lishman A W 1985 Fertility in the Afrikander cow. 2. Ovarian recovery and conception in suckled and non-suckled cows postpartum. Animal Reproduction Science 8: 315.

Williams G L 1990 Suckling as a regulator of postpartum rebreeding in cattle: a review. Journal of Animal Science 68: 831.

Williams G L and Griffith M K 1995 Sensory and behavioural control of gonadotrophin secretion during suckling-mediated anovulation in cows. Journal of Reproduction Fertility 49 (Suppl 1): 463.

Yavas Y and Walton J S 2000 Postpartum acyclicity in suckled beef cows: a review. Theriogenology 54: 25.

Zicarelli L, Esposito L, Campanile G, Di Palo R and Armstrong D T 1997 Effects of using vasectomised bulls in artificial insemination practice on the reproductive efficiency of Italian buffalo cows.  Animal Reproduction Science 47: 171.

Received 4 March 2012; Accepted 31 March 2012; Published 7 May 2012

Go to top