Relationship Between Ovarian Activity and Energy Status During the Early Postpartum Period of High Producing Dairy CoWS1,2

c.

R. STAPL~ and W. W. THATCHER

Dairy Science Department Institute of Food and Agricultural Sciences University of Florida Gainesville 32611

J. H. CLARK Department of Animal Sciences University 01 Illinois Urbana 61801

ABSTRACT

serves for milk production the first 2 wk of lactation, than cows cycling prior to d 40. (Key words: energy balance, lactation, estrus)

The effect of energy status upon ovarian activity during early lactation was assessed in 54 multiparous Holstein cows. Dry matter intake and milk yield were measured daily from parturition through 9 wk of lactation. Milk composition and body weight were measured weekly during this time. Energy balance corrected for body weight loss was calculated weekly. Blood was collected via tail vein three times weekly and plasma analyzed for progesterone and nonesterified fatty acids. Fifteen cows were anestrus for the 9 wk based on their plasma progesterone «1 nglml). These cows were compared with two cycling groups, one group of 25 cows showing corpus lute urn activity within 40 d after parturition and a second group of 14 cows showing corpus luteum activity between 40 and 60 d postpartum. Anestrus cows ate less feed, produced less milk, and lost more body weight, resulting in a more negative energy status than cycling cows. Differences in energy balance among cow groups were greatest the first 3 wk postpartum. Anestrus cows and cows showing corpus luteum activity between d 40 and 60 obtained more energy from body re-

INTRODUCTION

Received JWle 9. 1989. Accepted September 25. 1989.. . lAorida Agricultural Experiment StaUon Jownal Senes Number 9554. 2supported in part by the Illinois Agricultural Experiment Station. 3To whom reprint requests should be made.

1990 J Dairy Sci 73:938-947

Homeorhesis, defined as the orchestrated or coordinated changes in metabolism of body tissues necessary to support a physiological state (l), may be applied to the interrelationship of lactation and ovarian activity of the early postpartum cow. A prioritized physiological state, lactation for the survival of the newborn, may be allowed to proceed at the temporary expense of the procreation of a future calf. This ordering of events, when taken beyond the accepted "temporary" time frame, results in an inefficiency of the production system (more days open) that is considered unacceptable. The physiological mechanism(s) associated with this cause and effect relationship have not been elucidated clearly. Two gross factors have been linked to the number of days between calving and normal ovarian activity of healthy cows: amount of nutrients delivered for the cows' metabolism [body tissue mobilization and DM intake; (30)] and quantity of milk produced (16, 31). Estimating energy balance combines these two factors into a possible assessment of the homeorhetic state of the animal. Using 13 cows, Butler et al. (3) found that energy balance during the first 20 d of lactation was related inversely (-.60) to days to normal ovulation. The purpose of this study was to examine the relationship of energy balance and ovarian activity of early postpartum dairy cows experiencing homeorhesis.

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ENERGY BALANCE AND RElURN TO OVARlAN AcrIVITY

MATERIALS AND METHODS

TABLE 1. Ingredient and chemical composition of experi· mental diet.

Multiparous Holstein cows at the University % of DM of lllinois were housed in a maternity barn 10 Item to 14 d prior to expected calving date. Cows Ingredient Com silage SS.OO were weighed the initial day in the barn. The 23.23 Ground sbelled com performance of 54 cows was monitored from Soybean meal 19.42 parturition through wk 9 of lactation. Cows that Umestone 1.17 experienced debilitating illness or injury were Oicalcium phosphate .38 .23 Sodium sulfate removed from the trial. While housed in the .45 Trace mineralized salt maternity barn, cows were fed rolled high Magnesium oxide .10 moisture corn supplemented with protein, minVitamins A and D .02 erals, and vitamins at 1% of body weight, corn O1emical silage for ad libitum access, and 4.5 kg of long 16.3 Crude protein. % OM alfalfa hay. Undegradable intake protein, % OM S.9 Within 24 h after calving, cows received ad Net energy of lactation libitum a diet of 55% com silage and 45% McaVkg 1.68 concentrate consisting of ground com, soybean Acid detergent fiber. meal, minerals, and vitamins (Table 1). The % DM 19.6 Calcium, % DM .70 diet was fed twice daily as a totally mixed Phosphorus. % OM .40 ration. Dry matter intakes were recorded daily. Magnesium, % OM .25 Feeds were sampled weekly, and OM (55·C for Potassium, % DM 1.05 48 h) was determined to maintain the proper Sulfur, % DM .22 forage to concentrate ratio. Feeds collected weekly were composited at 4-wk intervals and assayed for CP (Kjeldahl) and ADF (9). Cows were milked twice daily and milk weights recorded. Each week, milk samples were col- P4 concentrations greater than 1 nglm] for more lected from two consecutive milkings (a.m. and than 2 consecutive sample days (short cycle) p.m.) and composited according to milk yield. and followed by subsequent sustained rises in Samples were analyzed for fat (Dairy Lab Ser- P 4 concentrations, or 2) sustained rises in P 4 vices, Inc., Dubuque, IA; Multispec A, infrared concentrations without a prior short cycle. milk analysis) and SNF (10). Cows were Cows were grouped into three preplanned reproductive statuses from which potential differweighed weekly prior to the a.m. feeding. Ten milliliters of blood were collected via ences in energy balance were tested. It was tail vein at approximately 1400 h each Monday, hypothesized that cows with distinctive differWednesday, and Friday after parturition until ences in timing of postpartum ovarian recrudesapproximately 63 d postpartum. Samples were cence would have marked differences in energy centrifuged at 5000 x g for 10 min. Plasma was balance. Cows were classified according to removed via micropipette and frozen until ana- their time of return to normal ovarian activity lyzed for nonesterified fatty acids (NEFA; (Table 2). Early responders (ER; n = 25 or 46% Wako Chemical, Dallas, TX) and progesterone of cows), Group I, showed corpus luteum ac(P4)' Progesterone concentrations in hepa- tivity within 40 d after parturition. Group 2 rinized plasma samples were measured with an contained cows showing corpus luteum activity assay system described by Knickerbocker et al. between 40 and 60 d postpartum and classified (14). An antiserum dilution of 1:40000 was as late responders (LR, n = 14 or 26%). Group used, and sensitivity of the assay was 31.2 pg 3 was composed of anestrus cows or nonper tube. Assays were conducted with 100 or responders (NR, n = 15 or 28%) during the first 200 J.Ll of sample. Intraassay and interassay 63 d postpanum. Energy status of cows was determined using coefficients of variation were 8.2 and 12.5%, respectively. Plasma P4 concentrations were the following assumptions and equations: used to indicate when the cow had returned to normal estrous cycles. Evidence of corpus luNet energy intake (NEI Mcal/wk) NE, of teum activity was defined as either: 1) plasma diet (McalIkg) (21) x DM intake (kg/wk).

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STAPLES ET AL.

TABLE 2. Age and incidence of health disorders of dairy cows differing in ovarian activity during the fIrSt 9 wk postpanum. Classification of ovarian activity I

ER

Item

Return to ovarian activity. d postpanwn 60 15

14

2 0 4

3 3 3

0

1 1

0 1

= late

RESULTS AND DISCUSSION

4.6

3.9

1

responder. NR

=

nonresponder.

Net energy of maintenance (NEro; Meal) = BW 75 x (.073 Mca1/k.g BW required for maintenance plus 10% for activity) (17, 21). Energy in milk (NEI; Mcal/wk) = milk yield (pounds) x ([41.84 x % of milk fat] + [22.29 x % SNF] - [25.58]) (28). Energy in body weight loss (NEBWL; Meal) = body weight loss (kg/wk) x 6 Meal of body tissue energy/kg of empty BWL (16) x 18% (estimate of inefficiency of converting 1 kg of body tissue reserves to I kg of 4% FCM) (19). Energy balance (EB) was calculated by the following equation for each cow on a weekly basis because cows were weighed weekly, and milk samples were taken and analyzed weekly. EB (Mcal/wk)

= NE[

NEBWL

NEro - NEI +

All data except P4 and NEFA concentrations in plasma were analyzed as a completely randomized design with sources of variation being group classification according to ovarian activity, cow (group classification), week, and week by group classification interaction. Single degree of freedom contrasts for treatment were I) cows returning to normal ovarian activity (ER and LR) versus cows not returning to normal Journal of Dairy Science Vol. 73. No.4, 1990

ovarian activity (NR), and 2) cows returning to nonnal ovarian activity within 40 d postpartum (ER) versus cows returning to normal ovarian activity between d 40 and 60 (LR).

Weekly least squares means of plasma P4 for the three classification groups are depicted in Figure 1. The average plasma P4 values for 63 d were 2.59, 1.39, and .52 ng/ml for ER, LR, and NR groups, respectively. Average day of first ovulation for ER was 21.9 ± 7.7. This is comparable to values in previous reports: 17.6 (25), 19.5 (13), 20.8 (7), and 23.9 (29) d. Duration of first postpartum estrous cycle ranged from 6 to 22 d. which is similar to the 9 to 28 d range of cycles observed by Fonesca et al. (7). Fifty-four percent of ovulating cows (n = 21 of 39) showed a short estrous cycle lasting an average of 10 d. The percentage of cows exhibiting a short estrous cycle was substantially greater than the 33% observed by Stevenson and Britt (25) involving 28 Holstein cows sampled twice weekly to detennine P4 concentration of plasma. Forty percent of ER cows showed no short estrous cycle but immediately started a normal cycle (defined as at least 17 d in length). Whitmore et al. (31) studied 396 ovulations of which 43% occurred without a detected estrus. Mean peak P4 concentration in blood plasma during first estrous cycle was reported to be less than that of second estrous cycle [3.7 vs. 4.7 ng/ml; (25)]. A similar pattern was observed for those ER cows that had two diestrous phases or two plasma P4 peaks within 63 d postpartum. Average plasma P4 peak for first estrous cycle was 5.95 ± 3.44 ng/ml, but plasma P4 peak for the second cycle was 8.79 ± 3.30 ng/ml. Thus, corpus luteum function was not maximal during the first estrous cycle. The percentage of anestrus cows observed in this study (28%) was more than the previously reported 10% (7 of 69) determined by King et al. (13) but similar to the 25.9% reported by Thatcher and Wilcox (26) who examined 1398 cows for 60 d postcalving. Because health disorders at the time of calving or during early lactation have negative effects on reproductive (4, 7) and lactational performance (27), incidence of health disorders is summarized in Table 2 for the three groups of cows classified according to ovarian activity.

ENERGY BALANCE AND RETURN TO OVARIAN ACfIVITY

Pneumonia was the only health disorder that was a greater problem among NR than ER and LR groups. Pneumonia always occurred with another health disorder: milk fever once and metritis twice. To determine whether the inclusion in the data analysis of cows experiencing health problems may have biased the results in some manner, an analysis with only healthy cows (n = 46) was done. Results were not different between the two data sets; therefore all cows were included. Thus, it does not appear that the lack of normal ovarian activity experienced by cows in this study was due to a higher incidence of health problems during the early postpartum period. Another factor shown to influence reproductive performance is age. Cows that had completed four or more lactations had more days to first service than younger cows (12). Average age of each group of cows is listed in Table 2. The average age of the ER and NR groups was 4.6 yr, but the LR group was only slightly younger, averaging 3.9 yr. Therefore, age probably did not account for differences in ovarian activity. During wk 1, all cows consumed feed at less than 2% of body weight with the NR group consuming the least (Figure 2). Thereafter, ER and LR cows, having normal ovarian activity. increased their feed intake more rapidly than NR cows with abnormal ovarian activity. By d 25, cows with cycling ovaries were consuming OM at a rate of 3% of their body weight, but

anestrus cows did not consume that quantity of OM until approximately 2 wk later. The NR group continued to lag behind other cows for the entire experiment and never reached the OM intake of 3.5% of body weight achieved by ER and LR groups. A slow increase in OM intake postpartum is commonly observed for cows that have poor milk production and reproduction. Coppock et aI. (5) reported that OM intake progressively increased for the first 16 wk of lactation before starting to decline. Because of the long time required by cows to reach peak feed intakes, Reid et aI. (23) concluded that appetite was the greatest limitation to large milk yields. The ER and LR groups consumed more (P.05) for cows that conceived. From the interrelationships between energy balance (Figure 7) and plasma P 4 concentrations (Figure 1), the marked deficit in early energy balance exerted a marked carryover effect on ovarian activity in the NR group. These cows failed to cycle until after 9 wk of lactation even though the energy balance of the three groups was the same by 5 wk postpartum. This prolonged carryover effect on reproduction is further substantiated by the observation that only 33.3% (5 of 15) of NR cows eventually conceived compared with 84 and 93% for ER and LR groups, respectively. The homeorhetic drive for milk production in dairy cows immediately after calving puts cows into negative energy balance. The partitioning of energy from the diet and from mobilization of body reserves for milk production and ovarian activity is highly regulated and appears to be influenced by energy status of lactating cows. The ER and LR groups of cows in a less negative energy balance than the NR group were able to restore ovarian activity during the first 63 d postpartum. In contrast. the NR group of cows, which were in a more negative energy balance, did not have the capability to consume as much dietary energy, produced less milk, and were more dependent on energy from body reserves to produce milk. As a consequence, their metabolic status inhibited recrudescence of postpartum ovarian activity within 63 d postpartum. Additional research is warranted to examine whether postpartum negative energy balance compromises ovarian follicular development or ovulation and subsequent corpus luteum development. The decline in plasma concentrations of NEFA were rather dynamic in the postpartum period but appeared to be unrelated to ovarian function in the present study. Feeding systems to minimize postpartum deficits in energy balance (e.g., increase in caloric density of the diet) and whether such management strategies alter ovarian follicular and corpus luteum dynamics need to be examined. REFERENCES 1 Bawnan. D. E., and W. B. Currie. 1980. Partitioning of nutrients during pregnancy and lactation: a review of Journal of Dairy Science Vol. 73. No.4, 1990

mechanisms involving homeostasis and homeorhesis. 1. Dairy Sci. 63:1514. 2 Bergbom, K. A., R. D. Allrich, and C. H. Noller. 1988. Energy balance and reproductive traits of postpartum dairy cattle. J. Dairy Sci. 71(Suppl. 1):171. (Abstr.) 3 Butler, W. R., R. W. Everett, and C. E. Coppock. 1981. The relationships between energy balance, milk production, and ovulation in postpartum Holstein cows. J. Anim. Sci. 53:742. 4 Callahan. C. J., R. E. Erb. A. H. Surve, and R. D. Randel. 1971. Variables influencing ovarian cycles in postpartum dairy cows. J. Anim. Sci. 33:1053. 5 Coppock, C. E., C. H. NoUer, and S. A. Wolfe. 1974. Effect of energy-concentrate ratio in complete feeds fed ad libitum on energy intake in relation to requirements by dairy cows. 1. Dairy Sci. 57:1371. 6 Dachir, S., R. W. Blake, and P. G. Harms. 1984. Ovarian activity of Holstein and Jersey cows of diverse transmitting abilities for milk. J. Dairy Sci. 67: 1776. 7 Fonesca, F. A., J. H. Brin, 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. 1. Dairy Sci. 66: 1128. 8 Fronk, T. J., L. H. Schultz. and A. R. Hardie. 1980. Effect of dry period overconditioning on subsequent metabolic disorders and performance of dairy cows. J. Dairy Sci. 63:1080. 9 Goering, H. K., and P. J. Van Soest. 1970. Forage fiber analysis. USDA Agric. Handbook 379, Washington, DC. 10 Golding, N. S. 1959. A solids-not-fat test for milk using density plastic beads as hydrometers. J. Dairy Sci. 42: 899. (Abstr.) 11 Hamudikuwanda, H., H. N. Erb. and R. D. Smith. 1987. Effects of sixty-day milk yield on postpartum breeding performance in Holstein cows. J. Dairy Sci. 70:2355. 12 Hillers. J. K., P. L. Senger, R. L. Darlington, and W. N. fleming. 1984. Effects of production, season. age of cow, days dry, and days in milk on conception to first service in large commercial dairy herds. J. Dairy Sci. 67: 861. 13 King. G. J., 1. F. Humik, and H. A. Robenson. 1976. Ovarian function and estrus in dairy cows during early lactation. J. Anim. Sci. 42:688. 14 Knickerbocker. 1. J., W. W. Thatcher, F. W. Bazer, M. Drost, D. H. Barron, K. B. Fincher, and R. M. Roberts. 1986. Proteins secreted by day 16 to 18 conceptuses extend corpus luteum function in cows. J. Reprod. Fenil. 77:381. 15 Laben, R. L., R. Shanks, P. J. Berger. and A. E. Freeman. 1981. Factors affecting milk yield and reproductive performance. J. Dairy Sci. 65:1004. 16 Marion, G. B., and H. T. Gier. 1968. Factors affecting ovarian activity after parturition. 1. Anim. Sci. 27: 1621. 17 Moe, P. W., W. P. Flatt. and H. F. Tyrrell. 1972. The net energy value of feeds for lactation. J. Dairy Sci. 55:945. 18 Moe, P. W., and H. F. Tyrrell. 1974. Observations on the efficiency of utilization ofmetabolizable energy for meat and milk production. Proc. Univ. Nottingham Nutr. Conf. Feed Manuf. 7:'1:1. Butterworth. London, Engl. 19 Moe. P. W., H. F. Tyrrell. and W. P. Flatt. 1971. Energetics of body tissue mobilization. J. Dairy Sci. 54: 548.

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estrus as an indicator of reproductive status in the dairy cow. J. Dairy Sci. 56:608. 27 Thompson. J. R.. E. 1. Pollak, and C. L. Pelissier. 1983. Interrelationships of panurition problems. production of subsequent lactation. reproduction, and age at fITst calving. J. Dairy Sci. 66:1119. 28 Tyrrell. H. F.. and J. T. Reid. 1965. Prediction of the energy value of cow's milk. J. Dairy Sci. 48:1215. 29 Villa-Godoy. A., T. L. Hughes. R. S. Emery. L. T. Chapin. and R. L. Fogwell. 1988. Association between energy balance and luteal function in lactating dairy cows. 1. Dairy Sci. 71:1063. 30 Wettemann, R. P.• K. S. Lusby, J. C. Garrnendia. M. W. Richards. G. E. Selk. and R. J. Rasby. 1986. Postpanum nutrition. body condition and reproductive performance of f1fst calf heifers. Page 314 in Anim. Sci. Res. Rep., Oklahoma Agric. Exp. Sm., Stillwater. 31 Whitmore, H. L .• W. J. Tyler, and L. E. Casida. 1974. Effects of early poslpanum breeding in dairy cattle. 1. Anim. Sci. 38:339.

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