Positive and negative effects of high energy consumption on reproduction in lactating dairy cows

Major changes are occurring in the reproduction of high producing lactating dairy cows. Reproductive management strategies to deal with these changes are discussed.

Changes in some reproductive measures in lactating dairy cows

Time to first ovulation

First ovulation is often delayed in lactating dairy cows with time to first ovulation averaging 33.3 ± 2.1 days in Holstein cows in the U.S.A. (compilation of 10 studies reported in Ferguson, 1996). This delay is generally attributed to the period of negative energy balance during the early postpartum period in dairy cattle, and a reduction in the pulsatile luteinizing hormone (LH) secretion needed to stimulate the final stages of follicle growth and estradiol production ( Savio et al., 1990; Staples et al., 1990; Beam and Butler, 1997; Lamming and Darwash, 1998; Roche et al., 2000; Butler, 2001).
Although delayed first ovulation is associated with negative energy balance, it is not as clearly associated with level of milk production.

Negative energy balance and inadequate follicular growth can explain a portion of anovulatory dairy cows but does not seem to be an adequate explanation for every case. Similarly, a simple relationship between anovulation and level of milk production does not appear to exist. More complex physiological models are needed to fully explain anovulation in dairy cows (Gumen and Wiltbank, 2002; Wiltbank et al., 2002).

Conception rate

Fertility is a complex trait that is likely to be related to numerous factors, including uterine infection, negative energy balance, urea concentrations in the blood, vitamins, fertility of sire, accuracy of estrous detection, insemination technique, etc. (Faust et al., 1988; Staples et al., 1990; Ferguson, 1996; Lamming and Darwash, 1998; Gröhn and Rajala-Schultz, 2000; Roche et al., 2000; Royal et al., 2000; Butler, 2001; Lucy,
2001; Moreira et al., 2001; Gong et al., 2002; Washburn et al., 2002; Lopez-Gatius, 2003; Santos et al., 2004a; Santos et al., 2004b). For example, increased double ovulation rate in high- producing dairy cows increases the chance of pregnancy, even though high milk production is expected to decrease the odds of an ovulated oocyte to produce a pregnancy. Thus, a simple relationship between milk production and conception rate seems unlikely.

Duration of estrus

Low rates of estrous detection are reducing reproductive efficiency on commercial dairy farms. Estrous detection rates in southeastern U.S. Holstein dairy herds have decreased from 50.9% in 1985 to 41.5% in 1999 (Washburn et al., 2002). However, studies have reported both negative relationships between level of milk production (Harrison et al., 1989; Harrison et al., 1990) and no relationship (Fonseca et al., 1983; Van Eerdenburg et al., 2002) using twice daily visual heat detection.

Duration of estrus in a group of lactating dairy cows was evaluated using continuous monitoring of all mounts (HeatWatch system, Lopez et al., 2004). Cows with milk production above the herd average (~ 88 lb/day) had shorter (P < 0.001) duration of estrus (6.2 ± 0.5 h) than cows with lower milk production (10.9 ± 0.7 h). This effect was not due to parity; primiparous and multiparous cows showed similar responses.

High producing cows (103 lb/day) had larger follicles (18.6 ± 0.3 versus 17.4 ± 0.2 mm diameter; P < 0.01) but lower circulating estradiol (6.8 ± 0.5 versus 8.6 ± 0.5 pg/ml; P < 0.01) compared to lower producing cows (71 ± 1.3 lb/day) (Lopez et al., 2004). Duration of estrus increased as peak estradiol concentrations rose (positive correlation, r = 0.57; P < 0.0001), but decreased as milk production increased (negative correlation, r = -0.51; P < 0.0001). Higher levels of milk production were associated with smaller follicular size (negative correlation, r = -0.45; P < 0.0001).High milk production was postulated to lead to decreased circulating estradiol concentrations, resulting in decreased duration of estrus.

Double ovulation rate

Double ovulation rate has been directly linked to milk production (reviewed by Wiltbank et al., 2000; Lopez et al., 2005a). Double ovulation rate appears to be the underlying cause of increased twinning rate in lactating dairy cows, with 93% of twins being nonidentical (Silvia Del Rio et al., 2004). Numerous factors have been recognized as possible regulators of twinning rates, including age of dam, season, genetics, use of reproductive hormones or antibiotics, ovarian cysts, days open, and peak milk production [reviewed in Wiltbank et al., 2000]. In a large study on risk factors for twinning, Kinsel et al. (1998) concluded, “the single largest contributor (> 50%) to the recent increase in the rate of twinning is the increase in peak milk production”. Other publications show similar relationships between milk production and double ovulation rate (Fricke and Wiltbank, 1999; Lopez et al., 2005a).

A dramatic inflection point in double ovulation rate has been shown as milk production increases above 88 lb/day; it is unclear what physiological changes above this critical value. The level of production within the 2 weeks prior to ovulation is the most influential (Lopez et al., 2005a). As with duration of estrus, the first postpartum ovulation differed from other ovulations, showing a high double ovulation rate that was unrelated to milk production (Lopez et al., 2005a).

Circulating steroids and steroid metabolism in lactating dairy cows

As discussed above, cows with higher milk production ovulate larger follicles but have lower circulating estradiol (Lopez et al., 2004) and progesterone concentrations (Lopez et al., 2005a). Other studies have reported similar changes in circulating hormones and size of ovarian structures in lactating cows (Ahmad et al., 1995; Inbar et al., 2001).

There appear to be two reasonable explanations for the disconnection between circulating steroid hormones and size of follicles and corpus luteum (CL). The first possible explanation is that follicles and CL are less steroidogenically active in lactating dairy cows. This could be due to insufficient levels of circulating stimulatory hormones, substrate for steroidogenesis, or intracellular steroidogenic pathways. The hypothesis that ovarian structures in lactating dairy cows have reduced steroidogenic output has not been investigated adequately to support or refute this hypothesis. The second, more likely explanation is that steroid hormone metabolism increases as milk production increases.

Circulating hormone concentrations are determined by rates of production and metabolism of the hormone. Increased feed consumption, such as during lactation, has been shown to alter circulating progesterone and excretion of progesterone (Parr et al., 1993a; Parr et al., 1993b; Rabiee et al., 2001a; Rabiee et al., 2001b). Liver blood flow and metabolism of progesterone and estrogen increased immediately after any amount of feed consumption in both lactating and non-lactating cows (Sangsritavong et al., 2002). Further, metabolism of estrogen and progesterone was much greater (2.3 X) in lactating than in non-lactating cows (Sangsritavong, 2002; Sangsritavong et al., 2002). The changes in estrogen and progesterone metabolism after feeding are immediate and appear to be related to acute changes in liver blood flow. In lactating cows, a continuous high plane of nutrition appears to chronically elevate liver blood flow and metabolism of steroid hormones to approximately double the amount observed in similar size and age non-lactating cows. These results indicate that even with a similar level of hormone production, there would be lower circulating hormone concentrations in lactating dairy cows.

Although we cannot rule out the importance of changes in steroidogenic production by luteal and follicular tissue, it seems reasonable that the changes in circulating estradiol and progesterone can be accounted for by increased rates of steroid metabolism in lactating cows. We have synthesized this information into a simplified working model. Lactating cows have greater energy requirements than non-lactating cows. The high feed consumption required to meet these requirements leads to a dramatic increase in liver blood flow (Sangsritavong, 2002; Sangsritavong et al., 2002) which leads to elevated metabolism of both estrogen and progesterone with a subsequent reduction in their circulating concentrations, despite high production of steroid hormones by the follicle or CL. Therefore, it makes sense that a higher producing cow would have a shorter duration of estrus because of increased steroid metabolism. Thus, this model provides a logical and likely explanation for the changes in duration of estrus, and for the paradox of lower circulating steroids but larger ovarian structures occurring in lactating dairy cows.

In addition, the model explains how elevated steroid metabolism due to high milk production could reduce fertility. The preovulatory follicle and oocyte would be exposed to a longer period of elevated LH pulses that could lead to ovulation of an overstimulated oocyte and reduced fertility (Ahmad et al., 1995; Ahmad et al., 1996; Revah and Butler, 1996). A reduced rate of progesterone rise following ovulation could also reduce fertility, as has been suggested by others (Folman et al., 1973; Ahmad et al., 1996; Dunne et al., 1999; Mann, 2001).

However, this model does not yet explain how very high milk production (> 88 lb/day) can produce dramatic increases in double ovulation rate. Our recent intensive study of hormonal changes associated with selection of single, double, or triple dominant follicles in lactating dairy cows demonstrates that reduced circulating estradiol near follicle selection is not responsible for multiple dominant follicles (Lopez et al., 2005b), as we originally proposed (Wiltbank et al., 2000). Nevertheless, circulating progesterone is decreased and LH and FSH are increased near the time of selection, making it possible that changes in hormonal metabolism may still have a role in this process. Future manipulation of reproductive function in lactating dairy cows will require clearer information on the precise effects of elevated steroid metabolism on reproductive physiology in lactating dairy cows.

Practical reproductive management implications

The next section will briefly suggest some practical implications and reproductive management strategies for problem areas.

Decreased duration of estrus due to high milk production

What does this mean on a commercial dairy farm? We used the data on duration of estrus versus milk production to estimate what would happen to heat detection efficiency for cows with different levels of milk production. If a cow is producing about 70 lb/day, a 4-time per day heat detection program will detect about 90% of cows that are in estrus. However, this same program (4 times/day) will only detect about 50% of cows in heat if they are producing above 100 lb/day. The results are even worse if heat detection is done only twice per day or once per day. It should be noted that all of the probabilities in this analysis were based on actual ovulation by the cows (detected by ultrasound). Some producers will say that high producing cows are not cycling; however, they are cycling normally. Instead, these cows are not detected in heat because of extremely short heat duration.

Increasing frequency of heat detection can help solve this problem. Many heat detection aids, such as tail chalk, to help find cows that are in showing heat when observers are not present. This can be critical because high producing cows are showing heat for 4 hours or less in many cases. Most dairy producers in the United States are incorporating timed AI programs, such as Ovsynch, into their reproductive management programs to get highproducing cows bred in a timely manner.

Treating anovular cows

Although level of milk production is not normally associated with incidence of anovulation, dairy producers still need to treat anovular cows. Generally, 20% of dairy cows will not be cycling by 70 days after calving. This percentage will increase with a high percentage of low BCS (2.5 or less) cows. Anovular cows need to be quickly assigned to a hormonal program (and possibly nutritional program if they have low BCS) that will start the cows cycling. An Ovsynch program alone is not the ideal treatment for anovular dairy cows. Use of a CIDR® (Pfizer, Inc., New York, NY) or estradiol should be incorporated into these programs for optimal results.

Increasing double ovulation rate (and twinning rate) with increasing milk production

From a practical standpoint, there may be little that we can do to change this trend. It seems clear that the main increase occurs after cows are producing about 90 lb/day. Thus, we must anticipate a dramatic increase in double ovulation rate in high producing cows which will result in an increased twinning rate for the cows that conceive. Management procedures take into account this increasing twinning rate if milk production is increasing. First, twin pregnancies must be diagnosed. Second, to management procedures should be adapted for cows that are likely to have twin births. Twinning cows will calve earlier (10 to14 days on average) and are likely to have more problems during the calving process. Cows at risk for twins are the highest producing cows during the previous lactation.

Decreasing conception rate due to higher milk production

As discussed above, many factors impact conception rate in lactating dairy cows, including higher milk production. On many farms, production level may be a fairly minor factor. The effect of milk production on fertility is dramatically amplified during hot weather. Increased body temperature during heat stress leads to decreased reproductive success, particularly early embryonic death.

Since reduced conception rates seem to stem from events during the first week after insemination, transferring a good quality embryo at 7 days after expected time of AI should improve reproduction. In a fairly large experiment, conception rate in the University of Wisconsin herd was compared for cows were bred by AI with those undergoing embryo transfer (ET). However, ET did not improve overall conception in lactating cows, suggesting other timeframes are also important in conception failures.

Many laboratories are experimenting with alterations to timed AI programs that may increase conception rates in high producing dairy cows. There are numerous intriguing possibilities, but data is insufficient to change recommendations at this time.

References

Ahmad, N., S.W. Beam, W.R. Butler, D.R. Deaver, R.T. Duby, D.R. Elder, J.E. Fortune, L.C. Griel, L.S. Jones, R.A. Milvae, J.L. Pate, I. Revah, D.T. Schreiber, D.H. Townson, P.C.W. Tsang, and E.K. Inskeep. 1996. Relationship of fertility to patterns of ovarian follicular development and associated hormonal profiles in dairy cows and heifers. J. Anim. Sci. 74:1943-1952.

Ahmad, N., F.N. Schrick, R.L. Butcher, and E.K. Inskeep. 1995. Effect of persistent follicles on early embryonic losses in beef cows. Biol. Reprod. 52:1129-1135.

Beam, S.W., and W.R. Butler. 1997. Energy balance and ovarian follicle development prior to the first ovulation postpartum in dairy cows receiving three levels of dietary fat. Biol. Reprod. 56:133-142.

Butler, W.R. 2001. Nutritional effects on resumption of ovarian cyclicity and conception rate in postpartum dairy cows. In: Fertility in the high producing dairy cow. Occ. Publ. Br. Soc. Anim. Sci. No. 26: pp 133-145.

Dunne, L.D., M.G. Diskin, M.P. Boland, K.J. O’Farrell, and J.M. Sreenan. 1999. The effect of pre- and post-insemination plane of nutrition on embryo survival in beef heifers. Anim. Sci. 69:411-417.

Erb, H.N. 1984. High milk production as a cause of cystic ovaries in dairy cows: Evidence to the contrary. Comp. Cont. Edu. 6:215-219.

Faust, M.A., B.T. McDaniel, O.W. Robison, and J.H. Britt. 1988. Environmental and yield effects on reproduction in primiparous Holsteins. J. Dairy Sci. 71:3092-3099.

Ferguson, J.D. 1996. Diet, production and reproduction in dairy cows. Anim. Feed Sci. Tech.5:173-184.

Folman,Y., M. Rosenberg, Z. Herz, and M. Davidson. 1973. The relationship between plasma progesterone concentration and conception in postpartum dairy cows maintained on two levels of nutrition. J. Reprod. Fertil. 34:267-278.

Fonseca, F.A., J.H. Britt, B.T. McDaniel, J.C. Wilk, and A.H. Rakes. 1983. Reproductive traits of Holsteins and Jerseys. Effects of age, milk yield, and clinical abnormalities on involution of cervix and uterus, ovulation, estrous cycles, detection of estrus, conception rate, and days open. J. Dairy Sci. 66:1128-1147.

Fricke, P.M., and M.C. Wiltbank. 1999. Effect of milk production on the incidence of double ovulation in dairy cows. Theriogenology 52:1133-1143.

Ginther, O.J., K. Kot, L.J. Kulick, S. Martin, and M.C. Wiltbank. 1996. Relationships between FSH and ovarian follicular waves during the last six months of pregnancy in cattle. J. Reprod. Fertil. 108:271-79.

Gong, J.G., W.J. Lee, P.C. Garnsworthy, and R.Webb. 2002. Effect of dietary-induced increases in circulating insulin concentrations during the early postpartum period on reproductive function in dairy cows. Reproduction 123:419-427.

Gröhn, Y.T., and P.J. Rajala-Schultz. 2000. Epidemiology of reproductive performance in dairy cows. Anim. Reprod. Sci. 60-61:605-614.

Grummer, R.R., and D.J. Carroll. 1988. A review of lipoprotein cholesterol metabolism: Importance to ovarian function. J. Anim. Sci. 66:3160-3172.

Gumen, A., J.N. Guenther, and M.C. Wiltbank. 2003. Follicular size and response to Ovsynch versus detection of estrus in anovular and ovular lactating dairy cows. J. Dairy Sci. 86:3184-3194.

Gumen, A., and M.C. Wiltbank. 2002. An alteration in the hypothalamic action of estradiol due to lack of progesterone exposure can cause follicular cysts in cattle. Biol. Reprod. 66:1689-95.

Hageman, W.H., G.E. Shook, and W.J. Tyler. 1991. Reproductive performance in genetic lines selected for high or average milk yield. J. Dairy Sci. 74:4366-4376.

Hansen, L.B. 2000. Consequence of selection for milk yield from a geneticist’s viewpoint. J. Dairy Sci. 83:1145-1150.

Harrison, R.O., S.P. Ford, J.W. Young, A.J. Conley, and A.E. Freeman. 1990. Increased milk production versus reproductive and energy status of high producing dairy cows. J. Dairy Sci. 73:2749-2758.

Harrison, R.O., J.W. Young, A.E. Freeman, and S.P. Ford. 1989. Effects of lactational level on reactivation of ovarian function, and interval from parturition to first visual oestrus and conception in high-producing Holstein cows. Anim. Prod. 49:23- 28.

Haughian, J.M., R. Sartori, J.N. Guenther, A. Gümen, and M.C. Wiltbank. 2002. Extending the postpartum anovulatory period in dairy cattle with estradiol cypionate. J. Dairy Sci. 85:3238-3249.

Inbar, G., D. Wolfenson, Z. Roth, M. Kaim, A. Block, and R. Braw-Tal. 2001. Follicular dynamics and concentrations of steroids and gonadotropins in lactating cows and nulliparous heifers. J. Dairy Sci. 84 (Suppl 1):465 [abstract].

Kinsel, M.L., W.E. Marsh, and P.L. Ruegg, and W.G. Etherington. 1998. Risk factors for twinning in dairy cows. J. Dairy Sci. 81:989-993.

Lamming, G.E., and A.O. Darwash. 1998. The use of milk progesterone profiles to characterise components of subfertility in milked dairy cows. Anim. Reprod. Sci. 52:175-190.

Lopez, H., D.Z. Caraviello, L.D. Satter, P.M. Fricke, and M.C. Wiltbank. 2005a. Relationship between level of milk production and multiple ovulations in lactating dairy cows. J. Dairy Sci. 88:2783-2793.

Lopez, H., R. Sartori, and M.C. Wiltbank. 2005b. Reproductive hormones and follicular growth during development of one or multiple dominant follicles. Biol. Reprod. 72:788-795.

Lopez, H., L.D. Satter, and M.C. Wiltbank. 2004. Relationship between level of milk production and estrous behavior of lactating dairy cows. Anim. Reprod. Sci. 81:209-223.

Lopez-Gatius, F. 2003. Is fertility declining in dairy cattle? A retrospective study in northeastern Spain. Theriogenology 60:89-99.

Lucy, M.C. 2001. Reproductive loss in highproducing dairy cattle: where will it end? J Dairy Sci. 84:1277-1293.

Lucy, M.C. 2000. Regulation of ovarian follicular function by somatotropin and insulin-like growth factors in cattle. J. Dairy Sci. 83:1635-1647.

Mann, G.E., and G.E. Lamming. 2001. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121:175-180.

McDougall, S., C.R. Burke, K.L. MacMillan, and N.B. Williamson. 1995. Patterns of follicular development during periods of anovulation in pasture-fed dairy cows after calving. Res. Vet. Sci. 58:212-216.

Moreira, F., O. Orlandi, C.A. Risco, R. Mattos, F. Lopes, and W.W. Thatcher. 2001. Effects of presynchronization and bovine somatotropin on pregnancy rates to a timed artificial insemination protocol in lactating dairy cows. J. Dairy Sci. 84:1646-1659.

National Research Council. 2001. Nutrient requirements of dairy cattle. 7th rev. ed., Natl. Acad. Sci., Washington DC.

Parr, R.A., I.F. Davis, M.A. Miles, and T.J. Squires. 1993a. Feed-intake affects metabolic-clearance rate of progesterone in sheep. Res. Vet. Sci. 55:306-310.

Parr, R.A., I.F. Davis, M.A. Miles, and T.J. Squires. 1993b. Liver blood flow and metabolic clearance rate of progesterone in sheep. Res. Vet. Sci. 55:311-316.

Peters, M.W., and J.R. Pursley. 2002. Fertility of lactating dairy cows treated with Ovsynch after presynchronization injections of PGF2a and GnRH. J. Dairy Sci. 85:2403-2406.

Pursley, J.R., M.R. Kosorok, and M.C. Wiltbank. 1997. Reproductive management of lactating dairy cows using synchronization of ovulation. J. Dairy Sci. 80:301-306.

Pursley, J.R., M.O. Mee, and M.C. Wiltbank. 1995. Synchronization of ovulation in dairy cows using PGF2a and GnRH. Theriogenology 44:915-923.

Pursley, J.R., M.C. Wiltbank, J.S. Stevenson, J.S. Ottobre, H.A. Garverick, and L.L. Anderson. 1997. Pregnancy rates per artificial insemination for cows and heifers inseminated at a synchronized ovulation or synchronized estrus. J. Dairy Sci. 80:295-300.

Rabiee, A.R., K.L. Macmillan, and F. Schwarzenberger. 2001a. Excretion rate of progesterone in milk and faeces in lactating dairy cows with two levels of milk yield. Reprod. Nutr. Dev. 41:309-319.

Rabiee, A.R., K.L. Macmillan, and F. Schwarzenberger. 2001b. The effect of level of feed intake on progesterone clearance rate by measuring feacal progesterone metabolites in grazing dairy cows. Anim. Reprod. Sci. 67:205-214.

Revah, I., and W.R. Butler. 1996. Prolonged dominance of follicles and reduced viability of bovine oocytes. J. Reprod. Fertil. 106:39-47.

Roche, J.F., D. Mackey, and M.D. Diskin. 2000. Reproductive management of postpartum cows.Anim. Reprod. Sci. 60-61:703-712.

Royal, M.D., A.O. Darwash, A.P.F. Flint, R. Webb, J.A. Woolliams, and G.E. Lamming. 2000. Declining fertility in dairy cattle: changes in traditional and endocrine parameters of fertility. Anim Sci . 70:487-501.

Sangsritavong, S. 2002. Studies of steroid metabolism in dairy cattle. Ph.D. Dissertation, Univ. Wisconsin, Madison.

Sangsritavong, S., D.K. Combs, R. Sartori, and M.C. Wiltbank 2002.. High feed intake increases blood flow and metabolism of progesterone and estradiol-17ß in dairy cattle. J. Dairy Sci. 85:2831-2842.

Santos, J.E., S.O. Juchem, R.L. Cerri, K.N. Galvao, R.C. Chebel, W.W. Thatcher, C.S. Dei, and C.R. Bilby. 2004a. Effect of bST and reproductive management on reproductive performance of Holstein dairy cows. J. Dairy Sci. 87:868-881.

Santos, J.E.P., W.W. Thatcher, R.C. Chebel, R.L.A. Cerri, and K.N. Galvao. 2004b. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Anim. Reprod. Sci. 82-83(Special Issue SI):513-535.

Sartori, R., J.M. Haughian, R.D. Shaver, G.J. Rosa, and M.C. Wiltbank. 2004. Comparison of ovarian function and circulating steroids in estrous cycles of Holstein heifers and lactating cows. J. Dairy Sci. 87:905-920.

Sartori, R, R. Sartor-Bergfelt, S.A. Mertens, J.N. Guenther, J.J. Parrish, and M.C. Wiltbank. 2002. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 85:2803- 2812.

Savio, J.D., M.P. Boland, N. Hynes, and J.F. Roche. 1990. Resumption of follicular activity in the early post-partum period of dairy cows. J. Reprod. Fertil. 88:569-79.

Silva Del Rio, N., B.W. Kirkpatrick, and P.M. Fricke. 2004. Observed frequency of monozygotic twinning in lactating Holstein cows. J. Dairy Sci. 87 (Suppl 1):65 [abstract].

Staples, C.R., W.W. Thatcher, and J.H. Clark. 1990. Relationship between ovarian activity and energy status during the early postpartum period of high producing dairy cows. J. Dairy Sci. 73:938- 947.

Van Eerdenburg, F.J.C.M., D. Karthaus, M.A.M. Taverne, I. Merics, and O. Szenci. 2002. The relationship between estrous behavioral score and time of ovulation in dairy cattle. J. Dairy Sci. 58:1150-1156.

Vasconcelos, J.L.M., S. Sangsritavong, S.J. Tsai, and M.C. Wiltbank. 2003. Acute reduction in serum progesterone concentrations after feed intake in dairy cows. Theriogenology 60:795-807.

Washburn, S.P., W.J. Silvia, C.H. Brown, B.T. McDaniel, and A.J. McAllister. 2002. Trends in reproductive performance in southeastern Holstein and Jersey DHI herds. J. Dairy Sci. 85:244-251.

Wiltbank, M.C., P.M. Fricke, S. Sangritasvong, R. Sartori, and O.J. Ginther. 2000. Mechanisms that prevent and produce double ovulations in dairy cattle. J. Dairy Sci. 83:2998-3007.

Wiltbank, M.C., A. Gümen, and R. Sartori. 2002. Physiological classification of anovulatory conditions in cattle. Theriogenology 57:21-52.

Xu, Z.Z., and L.J. Burton. 1999. Reproductive performance of dairy heifers after estrus synchronization and fixed-time artificial insemination. J. Dairy Sci. 82:910-917.

Authors

University of Wisconsin-Madison

University of Wisconsin-Madison